Project acronym:
MIDAS
Grant Agreement:
603418
Deliverable number:
Deliverable 4.2
Deliverable title:
Gap analyses of existing data to determine what
future sampling is required and to provide support
for ecological modelling from selected study
regions
Work Package:
WP4
Date of completion:
14 December 2014
BIOGEOGRAPHY AND CONNECTIVITY IN DEEP-SEA HABITATS WITH MINERAL RESOURCE
POTENTIAL
A GAP ANALYSIS
Table of Contents
Executive Summary
1
3.1.5 CCFZ: Nodules
24
Current state of knowledge
3
3.1.6 CCFZ: Gaps to our knowledge
26
1. Introduction
7
KNOWLEDGE GRID for CCFZ
28
1.1 Aims and objectives of study
7
3.2 SMS – MIDAS areas from the Mid Atlantic Ridge
29
1.2 Study areas
7
3.2.1 Patterns of biogeography
30
1.3 Methodology approach undertaken in this study.
7
3.2.2 MAR-Vent systems: Gaps to our knowledge
30
Knowledge Grids
8
3.3 Non-active vents and non-vent hard substratum sites
31
2. General considerations - rarity
9
3.3.1 Current Knowledge: Biogeography of major faunal groups
31
2.1 Rarity in deep-sea samples
9
KNOWLEDGE GRID for MID ATLANTIC RIDGE - Vent systems
32
2.2 The rarity-endemicity issue
9
3.3.2 MAR – non-vent and off vent environments: Gaps to knowledge
33
2.3 Rarity, sampling and appropriate scales of study
9
Cnidarian megafauna–Case study 3
34
2.4 How to deal with rare species in a mining environment?
9
KNOWLEDGE GRID for MID-ATLANTIC RIDGE - Non-vent environments
35
2.5 Discussion and Conclusions
13
3.4 Methane hydrate – Svalbard margin and Black Sea
36
Rarity and deep-sea sampling: Case study 1:
14
3.4.1 Svalbard margin.
36
3. Study areas: current biogeographic knowledge and gaps
17
KNOWLEDGE GRID for SVALBARD MARGIN
37
3.1 CCFZ – sediment nodule fields
17
3.4.2 Black Sea
38
3.1.2 Physical and biogeochemical gradients in the CCFZ
17
4. Modelling
39
3.1.3 Scales of habitat heterogeneity
18
5. General discussion
39
3.1.4 Molecular approaches
18
6. Conclusions
40
3.1.5 Patterns of biodiversity in the CCFZ
20
6. References
41
Macrofauna – Case Study 2
21
MIDAS: WorkPackage 4– deliverable 4.2. This report should be quoted as: Paterson,G.L.J., Menot, L., Colaço, A. Glover, A.G., Gollner, S., Kaiser, S., Gebruk, A.V., Janssen, A., Silva, M. C. A.,
Janssen, F., Sahling, H., Felden, J., Martinez, P.A. 2014. Biogeography and connectivity in deep-sea habitats with mineral resource potential–gap analysis. Deliverable 4.2. MIDAS. 45pp.
12 December 2014
BIOGEOGRAPHY AND CONNECTIVITY IN DEEP-SEA HABITATS WITH MINERAL RESOURCE POTENTIAL: A GAP ANALYSIS
Executive Summary
Determining the environmental impact of mineral extraction depends on the knowledge, information and data available. The deep sea remains our least explored and also our largest
environment on the planet. It follows that a considerable level of knowledge will be required to assess and manage sustainably exploitation of resources found in the deep sea. This report is an
investigation identifying the fundamental gaps in our understanding of the distribution of the organisms which inhabit the various deep-sea habitats currently being explored as potential sites
for mineral extraction. Understanding the biogeography of deep sea biota, the spatial distribution of life, is an essential first step in assessing the risks that extraction will pose. Knowing the
distribution of an organism is at the heart of assessing the likelihood that human activities will ultimately lead to its extinction.
In this report we undertake a gap analysis of current
biogeographic knowledge of four sites where deep-sea
mining may take place: massive sulphide deposits on the
Mid-Atlantic Ridge; nodule fields in the Central Equatorial
Pacific, methane hydrate fields in the areas off Svalbard in
the Arctic Ocean and in the Black Sea.
Gap analyses in this context is taken to mean an assessment
of the current understanding of biogeography, what data
are available to assess distribution patterns and what
information needs to be gathered to address any gaps. The
study focuses on the benthic fauna, looking at the various
size groups and the information known. The pelagic system
is not dealt with.
We present three case studies which highlight different
issues related to the biogeography of deep-sea organisms.
The first deals with rarity, the widespread observation that
a sizable proposition of the fauna collected is represented
by species with only one or two individuals. An analysis
indicates that while increased sampling can provide greater
information on whether species are really rare or merely
undersampled, practically no amount of sampling will be
able to solve this riddle. Ultimately it will be for regulators
to decide whether the risk of extinction of rare species is
acceptable.
The second case study attempts to use existing data to see
if it is possible to determine whether the fauna associated
with the nodules fields of the Pacific is widespread or
changes with distance. The initial results based on
macrofaunal polychaetes and meiofaunal nematodes
indicated that the species assemblage changes with
distance. If this is supported by further study then it would
mean that extensive mining in one area may well pose a
higher risk to the species which occur. It is therefore
important to know the local distribution of species.
However, the case study also indicated that the high
numbers of rare species may bias the results so further
study and sampling is needed.
The third case study looks at what is known about epifaunal
cnidarian species which are widespread but occur at low
densities. One of the species is the octocoral Corallium,
which occurs on non active and non-vent hard substratum
sites. It is important that we gain a better understanding of
the underlying factors governing epifaunal distribution in
order to assess whether the search for and exploitation of
one economic important resource could impact on another.
Understanding the species distributions of this group would
also provide information on what conditions are required
for epifaunal species to settle and grow.
General conclusions
Spatial coverage of sampling programmes.
The range of scientific, i.e. research-led, sampling
programmes to the various areas differs quite markedly.
There is little known about the biota of the methane
hydrate fields off Svalbard, while other sites have been
subject to varying degrees of study. Perhaps the best
investigated are the MAR vent sites TAG – most visited,
Lucky Strike – best studied and both have been visited on a
fairly regular basis since their discovery in the late 1980s.
The recurrent observation with all areas is that we lack
good data on the distribution of biota on many scales from
local (i.e. within habitats), regional (between habitats found
within a site or claim area) and on a basin scale. Stratified,
co-ordinated sampling programmes will be needed to
address this gap. The road map suggested by German et al.
(2011) highlights the need for academia and industry to
continue to work together to address key issues such as
extinction of rare species and potentially of isolating
populations. Such collaborations will go some way towards
addressing the gaps highlighted.
Taxonomic coverage and resolution of different biota.
Taxonomy is the key to understanding the distribution and
biogeography of biota. Megafauna generally have been
better studied and their taxonomy is at a more advance
stage than for most of the other groups. Nevertheless,
many megafaunal species, even well known ones, lack any
molecular assessment. In general population studies aimed
at determining connectivity have only been attempted with
abundant species but for most species their populations are
too small and widely dispersed to be able to collect enough
individuals to undertake meaningful population genetic
surveys. Modern genetic methods may be able to address
this problem but such methods have not been deployed in
current surveys.
1
Taxonomic resources, specifically trained people, continue
to be a limiting factor despite the rise of molecular tools.
The reasons for this have been the subject of much debate
and will not be repeated here but within the deep sea one
reason is the shear scale of the species richness that
sampling reveals. For smaller macrofauna, meiofauna and
taxa, such as Foraminifera, the numbers of species
recovered from a sampling programme can be into the
hundreds or thousands. In the past this has led to a more
ecologically focused approach which has concentrated
more on the identification of samples and much less on the
classification and formal description of species. The result
has been that formal taxonomy lags behind discovery and
ecological analyses, creating a major gap in our
biogeographic knowledge of deep-sea biota. And now, as
we stand on the brink of commercial exploitation of
deep-sea resources, we cannot say with any degree of
certainty what the risk of extinction will be for even large
charismatic megafaunal organisms.
Table 1. RAG assessment of biogeographic knolwedge of MIDAS sites being explored for mineral respources.
Vents
Megafauna
For some areas there is a considerable amount of data
available in the scientific literature. Vents megafauna being
the most studied. However, despite over four decades of
research in some of the MIDAS study areas the data remain
patchy and scarce. The Internatonal Seabed Authority have
developed a central database for collating information
which will serve as a much needed source of data for future
studies. At all times strong data management will be
2
Svalbard
seeps
Black Sea
N/a
Meiofauna
?
Microbial:
Protista
Microbial:
Bacteria
Microbial:
Archaea
Good
knowledge
with ability to
make
informed
predictions
s
CCFZ
N/a
Macrofauna
To reverse this both academic and commercial programmes
need to collaborate and develop robust taxonomic pipelines
which will result in consistent identification of species. Such
an infrastructure will need to include both traditional
morphological assessments as well as the application of
genetic tools and will need to use web-based approaches to
disseminate this information in a timely way. Decades of
work in various different habitats has shown that without
adequate resources to establish and run taxonomic
pipelines, no further work on the taxonomy of species will
be carried out. The critical data needed to assess risk of
extinction will not be generated.
Data availability.
Off vents
Useful data
available but
fundamental
gaps remain
Little or
primary
information
only
essential to ensure that data being produced are
appropriate and fit for purpose.
Collections of specimens from previous studies, both
commercial and academic are scattered across a variety of
institutions. It can be difficult to determine where the
material is. Some form of metadata catalogue would assist
in keeping track of important collections.
As commercial exploration activities increase in intensity,
good protocols will be needed to ensure that
samples/specimens are stored in recognised
collection-based institutions and made available for study.
Again resourcing for this activity needs to be built into the
commercial and academic programmes. Specimens are the
only way to verify the presence of a species at a particular
place in space and time and therefore are an important part
of the environmental auditing process.
Current state of knowledge
difficult to make convincing predictions as to the impact of
mining on species.
The RAG assessment (Red, Amber and Green) is based on
analyses of current knowledge of the biogeography of
different organism groups and the MIDAS sites (Table 1). It
is meant as a quick assessment of the current state of
understanding.
Green status means that the taxonomic knowledge is robust
and that it is possible or could be possible to make informed
predictions as to the impact of mining.
Red status means that the only sources of data and
information are in primary scientific publications and that
the coverage of the investigations undertaken are limited. It
is not possible to make any realistic predictions on the
impact of mining.
Only the megafauna associated with vent sites have been
well enough studied for an informed assessment of their
biogeography which could be used to assess mining impacts
on species populations. Most of the other faunal groups
and areas require considerably more research before we
are able to make informed assessments of impacts.
Amber status indicates that study of the particular
taxonomic group at a particular site is more comprehensive,
more than just primary data are available. But there are
significant gaps in biogeographic knowledge such that it is
3
BIOGEOGRAPHIC KNOWLEDGE GAPS WHICH IMPACT ON ENVIRONMENTAL ASSESSMENT AND SUSTAINABLE MANAGEMENT
1) Spatial coverage of sampling programmes.
Gap
Mitigation Actions
Priority
Information is insufficient for comprehensive analyses of most taxa likely to be affected by
mineral extraction irrespective of site.
Focused biological cruises coupled with stratified sampling programme across a range of
spatial scales.
Better co-ordination between teams undertaking exploratory work and research projects.
Coverage is patchy dependant on site and taxon.
Emphasis on obtaining a better taxon sampling using a range of gears.
High to
Medium
Insufficient information or data to determine linkages between different habitats, such as
sea mounts and other hard rock surfaces.
Sampling across different habitats not just those of immediate economic interest.
Medium
In large habitats such as abyssal plains and MAR off vent and non-vent environments, too
little is known of the pattern of distribution at different spatial scales which is the first step
towards identifying the underlying ecological drivers .
Targeted research including multidisciplinary cruises comparing Massive Sulphide Deposits
(MSD) with surrounding hard substratum habitats.
High to
Medium
In areas where mining claims have already been established – MAR and CCFZ – there is
little incentive for the different contractors to co-ordinate and share data, although some
now do.
Regulatory bodies should play a more constructive role in co-ordinating between contractors
and establish protocols for the sharing of non-commercial scientific data between contractors,
academia and NGOs.
High to
Medium
High
2) Taxonomic coverage and resolution of different faunistic elements.
Taxonomic knowledge needs to be developed as in only a few groups is there sufficient
biogeographic information.
Ensure taxonomic standards across all actors, particularly contractors, though workshops,
create a taxonomic data portal, encouraging publication of taxonomic results, develop a
taxonomic clearing mechanism which links taxonomic resources with teams needing specialist
support.
High
Molecular approaches linked to morphology and morphotypes need to be applied.
Molecular approaches need to be built into the taxonomic data pipeline. Linking molecular
data to morphotypes, where applicable, will enable previous studies and the taxa collected to
be linked more unequivocally to future identifications.
High
Developing infrastructure such as a clearing mechanism and a data sharing portal will support
taxonomic efforts and maximise existing resources.
High to
medium
Resolving OTU identifications, particularly intercalibrating between different studies and
between species identified using molecular methods will maximise the taxonomic resources
and improve resolution.
High
Better co-ordination between taxonomists, ecologists and the contractors is needed to
maximise existing taxonomic resources.
Resolution of most smaller elements of the biota, including the microbial, is at the level of
(M)OTU. This is a major impediment to understanding the distribution of biota.
4
3) Data availability
Gap
Mitigation Actions
Priority
Considerable amounts of data may be ‘hidden’ within grey literature – contract reports or
unpublished surveys. Such data are effectively unavailable.
Create a data portal to release non-commercial scientific data. The ISA would be the obvious
organisation to undertake this for the areas with mining claims.
Medium
Specimens, here considered the primary element of biogeographic data, are also
scattered, often difficult to access.
A metadata catalogue or holdings indicating what material is held where and what its status is in terms
of identification would be a useful resource.
Medium
Intercalibration of specimens is difficult and there is no mechanism or incentive for
contractors to join with researchers to produced unified datasets.
Develop appropriate taxonomic infrastructure as outlined above. Fund taxonomic intercalibration
workshops to produce unified datasets and publishable taxonomic keys and descriptions.
High to
medium
MIDAS sites
Clarion–Clipperton Fracture Zone nodule fields
CCFZ: High resolution studies to determine spatial patterns of species distributions. It is
important to understand how species are distributed across different habitats within claim
areas, between claim areas and in the APEIs.
Focused biological cruises by contractors and the research community.
Co-ordinated exchange of information.
Ensure the use of the ISA database.
High
CCFZ: Lack of basin-wide species level datasets.
Encourage contractors to make non-sensitive data available via ISA.
High
CCFZ: Lack of taxonomic consistency.
1) Create taxonomic clearing system and centralise taxonomic depository.
2) Training .
3) Taxonomic exchange programmes to improve capacity among actors.
High
CCFZ: Nodule fauna–is it endemic to nodules or found on other metal rich habitats such
as seamount crusts?
Sample seamounts within and beyond CCFZ.
High
CCFZ: Epifauna found in the CCFZ– does it also occur on hard surface areas such as
seamounts?
Focused sampling of megafaunal groups, particularly for molecular analyses. Develop cruise
programmes to visit both types of habitat. Many claim areas also have a range of seamounts so targeted
cruises could be planned..
High
CCFZ: Virtually nothing is known about protistan taxa such as ciliates, flagellates etc. The
importance of this obvious gap in knowledge is also unknown.
Molecular eDNA may be the only way to determine the biodiversity of such groups. Determining their
role in the ecosystem is also problematic and may depend on molecular approaches.
High to
medium
CCFZ: Microbial diversity and distribution.
Considerably more sampling is needed to understand the distribution of bacteria and archaea across the
CCFZ. Their function both in nutrient and metal cycling is important and needs to be elucidated.
High to
medium
CCFZ: Identifying the drivers for biogeographic patterns in the CCFZ
Integrating ecological data, e.g. productivity, with phylogenetic information from key species to identify
the historical-evolutionary processes and the ecological drivers.
High to
medium
5
MAR: Hydrothermal vents sites
Gap
Mitigation Actions
Priority
MAR: There have been few studies focussed on meiofauna diversity and distribution –
mostly in the Pacific and some from reduced sediments.
Targeted sampling – within mussel beds and tube thickets.
High to
medium
MAR: Little is known about microbial protistan biodiversity. Sampling hard surfaces is
difficult and new collectors may need to be engineered to optimise collection of these
taxa.
Targeted sampling across various habitats and zones within and between vents.
High to
medium
MAR: Increase molecular taxonomic knowledge and population studies of all taxa.
Establishing standard sampling and processing protocols to be used by academic research and
contractors.
High
MAR: Greater sampling coverage along the MAR and within the claim areas is needed to
be able to establish biogeographic patterns and distributions at different scales.
Co-ordinate research and exploration programmes and encourage academic and contractor
collaboration.
High
MAR: Off-vent and non-vent areas
MAR: There is no coherent understanding of the distribution of fauna from the sediment
habitats away from active vents and how it relates to sediment fauna from surrounding
abyssal and continetal habitats.
Stratified sampling combining AUV, ROV and tethered samplers from the claim areas and from areas
outside on the MAR
High
MAR: There is little understanding of the ecological drivers of the biogeographic patterns
of species associate with both hard rock and sediment habitats.
Targeted multidisciplinary research projects focused on off-vent sites, bringing together academia and
contractors.
High to
medium
MAR: molecular data is not available for most mega, macro and meiofauna which
impedes the ability to determine connectivity and distribution.
Establish molecular sampling/subsampling as a standard protocol for future work.
High
Svalbard: Methane hydrates
Svalbard: Intiatial investigations point to similarities between the Svalbard sites and those
from the Håkon Mosby mud volcano and Norwegian margin. However, different
chemosynthetic sites often have unique combinations of species so more intensive study is
needed to detemine the relationship and distribution patterns of the fauna.
6
Comprehesive sampling, including for molecular analyses will provide
Medium
1. Introduction
This study assesses the current state of the art in relation to our knowledge of the distribution and biogeography of the fauna from areas rich in deep-sea mineral resources. The aim is to
identify gaps, suggest future research priorities and to inform monitoring strategies being developed for these areas.
1.1 Aims and objectives of study
Knowledge of the distribution of organisms within and
between the sites of potential commercial interest and the
surrounding region is crucial in developing management
plans. Without such knowledge it becomes almost
impossible to determine the impact of resource extraction
on a regional scale. In effect how likely is it that such
activities lead to the permanent extinction of species?
2) Taxonomic coverage and resolution of different faunistic
elements. The aim is to determine whether all the
ecological actors had been sufficiently analysed. This aspect
also included whether there were any genetic analyses.
Here we assess whether taxonomic coverage and resolution
is sufficient to analyse biogeographic patterns and
1.2 Study areas
The main areas under consideration are the Mid-Atlantic
ridge hydrothermal systems , the Clipperton–Clarion
Fracture Zone polymetallic nodule fields in the Central
Pacific, methane hydrate fields in the Arctic and Black Sea.
All of these areas are likely to be regions where commercial
exploitation of mineral resources is planned. Figures 1 and 2
show the study sites.
1.3 Methodology approach undertaken in this study.
In this study we employ the term gap analyses to mean an
assessment of the fundamental data need to provide
information for management such that there is a good
understanding of the distribution of species and what
impact extraction of resources would have on species
affected. The information required could be both factual as
gained by analyses of samples or based on probabilistic
models together with the appropriate error terms.
The analyses undertaken followed the following steps:
1) Spatial coverage of sampling programmes in relation to
the key areas under investigation. Here we assess gaps in
the geographic coverage what has been termed the
Hutchinsonian perspective
Figure 1. MIDAS Study areas. Areas of particular focus for WP4: 14) CCFZ - nodules; 9-12) Mid-Atlantic Ridge - ; 1,2,5)
Black Sea and N. Arctic – methane hydrates.
7
connectivity between populations. This has been called the
Linnean perspective
3) Data availability. Given that in many of the study areas
research is undertaken by different teams from different
institutions and in some areas, such as the CCFZ, work is
undertaken by different contractors we assess how easy it is
to access data being produced. Assessing data coverage is a
necessary first step in developing predictive models.
Modelling is seen as a way of dealing with the large spatial
scales present in some of the sites and the problems of
adequately sampling in such an environment.
Knowledge Grids
As a means of summarising the understanding and
availability of data, a knowledge grid has been developed
for each of the main environments dealt with in this report.
The grid is composed of different taxonomic groups as
columns across the top–megafauna, macrofauna, etc.; with
a series of subject categories as rows. The categories
assessed were as follows:
Taxonomy
Taxonomic knowledge: this is an assessment as to what
level of taxonomic information is available to undertake
biogeographic studies.
Taxonomic resolution: this is a measure of the taxonomic
maturity. Are the taxa well classified and described? Or are
they only classified as an Operational or Molecular
Taxonomic Unit (OTU – MOTU), i.e. species 1, species b, etc.
Keys: in particular whether the data are available in original
primary sources or whether there are keys and large
revisions or monographs available.
Taxonomic information availability: in what form is the
taxonomic information available–primary sources, scientific
literature, on-line and what mechanisms, other than
publication in the scientific literature, will help people
exchange taxonomic information.
Sampling data coverage
Standards and protocols: are samples being taken using
similar methods between the different teams undertaking
surveys and primary research studies?
Biogeography
(in this study it is ecological aspects of biogeography which
are the focus)
Information and data availability: are there current,
available biogeographic analyses with suitable data already
available? Or if not are there any data with which to
undertake relevant biogeographic analyses?
The study focuses on the benthic fauna, looking at the
various size groups and the information known. The pelagic
system is not dealt with in this study.
Sampling: what kind of sampling is currently generating
taxon-based data?
Sample coverage: how comprehensive are the sampling
programmes – any particular gaps?
Molecular sampling: are samples for molecular analyses
being collected? Is this linked to morphological taxonomic
analyses or purely molecular such as eDNA studies?
Figure 2. MIDAS WP4 sites: CCFZ nodule fieds (image IFREMER); Hydrothermal chimney at Rainbow vent, MAR (image IMAR/DOP) ; MAR non-ventcoral garden Menez Gwen (image
IMAR/DOP); Black Sea bacteria carbonate mounds (image AWI); Arctic methane seeps (image AWI).
8
2. General considerations - rarity
In assessing biogeographic patterns, dealing with the question of rarity becomes a major challenge; one which is seldom really dealt with in the deep-sea literature. The long tail of rare species
associated with samples is considered to be an emergent property of the deep-sea ecosystem. However, in trying to determine ecological impacts some regard as to this challenge has to be
made. Effectively, the question will be asked – What is the likelihood that exploitation of mineral resources will lead to the extinction of species and that those species will be the rare or least
abundant ones? Or is this rarity really an artefact due in part to the huge size of the ecosystem and our ability to sample it effectively?
2.1 Rarity in deep-sea samples
In the following sections we discuss the implications of
rarity on assessing exploitation of resources. Rarity and
what it might mean in terms of biogeographic analyses and
subsequent environmental management are discussed.
2.2 The rarity-endemicity issue
A major characteristic of many species-rich habitats is that
the assemblage comprises a large number of species
represented by one or two individuals. In the deep sea
benthic samples are characterised by a long ‘tail’ of such
species (see Fig.2). In a study of hydrozoan and anthozoan
‘coral’ species found on the hard surface habitats around
the Azores, Braga-Henriques et al. (2013) reported that
30% of the 164 species recorded had only one or two
records (Fig 2). Collins et al. (2012) reported that 80% of the
fauna recovered from the vent systems in the Manus Basin
off Papua New Guinea were represented by 5 or fewer
individuals.
This long tail of species with few individuals is a major
characteristic of deep-sea diversity. However in terms of
assessing biogeography and connectivity the potential rarity
of such species posses a major question in such studies - are
such species actually rare or just undercollected? This is the
‘rarity’ problem (Gaston, 1994).
Rarity in this context is not the same concept as endemism.
Rare species can be widespread and endemic species can be
abundant. The problems and challenges to defining rarity
involve sampling intensity and variability in abundance –
the higher the errors in measuring these factors the
less confidence the rarity estimates return.
2.3 Rarity, sampling and appropriate scales of
study
Sampling efficiency is a particular issue with
deep-sea samples. In sediment environments such
as the CCFZ, quantitative sampling devices, such as
box corers, sample a small area of the ocean floor
and as a result large numbers of replicates are
needed to adequately sample one area. The
intensity of the sampling required places a heavy
burden on resources which is accentuated in some
deep-sea settings where faunal abundance is very
low. Use of the new generation of epibenthic
sledges can collect considerably larger samples.
They do not necessarily collect the same elements
of the fauna compared with corers. Such samplers
are also qualitative. Furthermore, in nodule areas,
the material collected can be quite damaged. So
though no apparatus will be representative for the
entire fauna, a combination of samplers will
probably provide more robust estimates of
biodiversity.
Rock environments such as MSD also are
problematic in terms of survey and sampling.
Extensive phototransects are available for the vent
areas themselves but off-vent areas are less
frequently surveyed. Collecting specimens requires
intensive use of ROVs. It is, therefore, difficult to
determine whether hard substrate fauna is rare or
merely undersampled. This challenge was also noted by Barsa
Henriques et al. (2013) for coral species around the Azores. They
suggested that it was not yet possible to be certain that records of
rare species were not artefacts of sampling despite 150 years of
sampling and study; increasing the sampling area may well result in
the discovery of more specimens of such species.
Molecular approaches provide an opportunity to shed some light on
connectivity between low abundance populations which may be
considered rare. But even here if sufficient material is not collected
then establishing rates of genetic exchange remains difficult if not
impossible to determine.
2.4 How to deal with rare species in a mining environment?
Rarity definitions are often based on a different scales, e.g.
definitions such as 'locally common but globally restricted' are often
used but must take into account skewed observations and temporal
change. Species life cycles can lead to changes in population sizes. A
more pragmatic approach may be to specify the actual area of
habitat being used or could be used by the species rather than some
arbitrary area encapsulating a range of habitats i.e. drawing a line
round a geographic region. Modelling may support such attempts
but more information on potential life styles, environmental
variables and biogeochemical settings will be required (see Section
4. Modelling).
These characterisations are difficult in the deep sea. As a first step it
is possible to assess the potential distributions of species and
therefore their status based on their occurrence in samples and the
degree of sampling undertaken.
9
Figure 2a. A typical species abundance graph showing the
long tail of macrofauna species with low numbers of individuals
from the Domes A nodule site in the Clipperton-Clarion
Fracture Zone, Central Pacific.
Figure 2b. Nematode species rank abundance curve from the
equatorial site of the EqPac study. Data from Brown (1998).
Figure 2c. Records of Anthozoa recorded from around the
Azores EEZ. The records are based on assessing literature
records, fishing bycatch returns and new sampling. In this
example the number of records indicate the rarity of the
species such that 50 species have only been recorded from
one sample. From Barga Henriques et al. (2013)
Figure 2d. Records of holothurian and asteroid species
recorded from the Mid-Atlantic Ridge. These records are based
on samples taken during the MAR-ECO programme. Data from
Gebruk (2008) and Dilman (2008).
10
Draft 11 Nov 2014
Table 2. Why it matters whether a species is rare. The impact of mineral extraction is compared against the different levels of species abundance. The
consequences of species loss at different geographical scales are estimated.
Species occurrence
Local scales (i.e. claim area, vent
site)
Regional Scale
Global scale
Common
Local extinction but populations elsewhere
remain viable
Some disruption to gene flow but no
major losses
No major losses
Locally abundant and widespread
As above
As above but local regional extinction
may occur changing the biogeography of
the species
No major losses
Locally abundant widespread but rare in other localities1
Local extinction but recovery and population
viability depends on where the species is most
abundant
Depending on population impacted the
effect may be to push a species to
non-viable levels
Potential loss or reducing the population of species to low
levels. Potentially placing species at risk.
Locally rare but widespread
Local extinction likely
Regional extinction may occur changing
biogeography
Globally rare may result in local but not total extinction
Local widespread, rare and restricted –endemic species
Local patches may survive if widely dispersed
within and beyond exploitation area
Threat of total extinction. At regional
scales it is a question of determining
habitat preferences and distribution
patterns
Species extinction possible.
Rare species
Locally restricted could result in total extinction
Extinction possible
Extinction possible
This is important in the context of local/claim area management. There may be regions of high richness with localised species which need to be preserved. Detailed sampling in the area is needed
1
11
2.5 Discussion and Conclusions
There are two aspects to rarity which need to be
considered. The first is whether extinction is a real
possibility and therefore acceptable in terms of the
sustainable management of mineral extraction. The second
is that if it is deemed acceptable what potential impact
could this have on ecosystem functioning.
Even with advances in molecular approaches or applying
modelling techniques, the rarity issue remains problematic
and it perhaps best categorised as potentially unknowable.
Pragmatically, given that research may be unable to resolve
the issue of whether extinction will be caused, it becomes a
matter for regulators to evaluate the risk.
12
Functionally what do such rare species contribute to
ecosystem function? Given they are found in low
abundance it is tempting to conclude that their contribution
is negligible. This however may be inaccurate and a result of
studying their distribution at an inappropriate scale (Jain,
2013; Mouillot et al 2013). The long tail of species with
single occurrences may appear to contribute little apart
from contributing to the high species richness characteristic
of a deep-sea sample. However, the large number of such
species may confer a degree of redundancy to the system
(Naeem, 1998). How a reduction in the number of species
would impact on the system's ability to recover or species
to recolonize remains unknown. In other ecosystems rare
species have been shown to have functional traits not
found in the common species and therefore contribute to
the functional diversity of the ecosystem. In some cases
rare species may support highly vulnerable functions.
Mouillot et al. (2013) suggest that such species may provide
the ecosystem with the functional robustness to adapt to
climate change or anthropogenic pressure.
Table 3 summarises the discussions around rarity and how it
relates to impact assessment and potential consequences
following exploitation.
Table 3. Rarity and its relevance at different scales following anthropogenic distrubance
Locally rare
Basin-scale rare
Globally rare
Local extinction threat – increase in
population patchiness
Loss of genetic diversity – potential
impact on functioning and gene flow
Serious threat of extinction
Detailed sampling across the claim and
preservation areas is essential to be able
to determine whether refugia contain
functioning populations
Need to know the distribution of all size
class elements at regional scales
Difficult to establish as the likely distribution
and occurrence are often unknown due to
lack of appropriate sampling
Knowledge Gap
Insufficient knowledge of small-scale
distributions and how this is related to
scales of physical heterogeneity
Insufficient molecular data to establish
population genetics
Insufficient information of biogeography
and connectivity basin scale studies
Understanding of species distributions
and population connectivity is poor to
non-existent
Lack of synthetic studies bringing together
information on distribution of different taxa
Reasons for gap
Detailed sampling is resource heavy
There is no regulatory mandate to do
this type of study
Taxonomic and ecological expertise is in
short supply
Funding is not sufficient to support this
intensive approach
Concentration by different contractors of
groups in selected areas
Lack of exchange of data
Molecular data are needed but often
difficult to get for certain faunal elements
Lack of data
Large-scale studies, particularly taxonomic
ones are time-consuming and require
financial support
Need taxonomic support and co-ordination
Consequences
Unable to determine whether refugia or
set aside areas will provide sufficient
protection
Unable to determine basin scale impacts
and to determine efficacy of regions of
special interest.
Unable to determine extinction levels on a
global scale because of poor baseline data
Local areas of refuge and no activity
areas
Regional reserved areas and no activity
zones
Restrictions on activity in zone where
endemic species are found
Impact
Relevance to deep
sea
Current mitigation
proposals
13
Rarity and deep-sea sampling—Case Study 1
An analysis of existing data is undertaken to assess
categories of species distribution. The aim is to determine:
1) how sampling may affect the designation of rarity to
species occurrence; 2) a more robust definition of rarity
and its consequences if an area is likely to be exploited; 3)
what steps might be take to reduce the impact of
exploitation on such species.
Table 1 summarises the impact that intensive exploitation
would have on species with differing levels of occurrence
at different scales. An attempt is made to provide a more
rigorous definition of species occurrence to try to separate
out different consequences of exploitation on their
survival at different spatial scales.
Method
Four datasets from the CCFZ were studied – two datasets
from sites east to west across the CCFZ (macrofaunal
polychaetes) and two from sites south to north (one of
polychaetes and one of meiofaunal nematodes). The
east–west samples were from previous studies: Domes A,
Echo and PRA, here termed CCFZ 1, and from three sites
sampled during the Kaplan study (ISA technical Report 3,
2008), here termed Kaplan, in the east, centre and west
(this latter site is very close to Domes A).South to North
sites were from the EqPac programme were assessed and
the numbers of species in the categories above were
counted.
Each species was assessed as to its occurrence in the
samples from each site, whether it also occurred in
different sites and if so how many. The relative abundance
of each species was also assessed to provide some
indication of whether the species occurred in the same
relative density in all samples and sites. Based on its
occurrence each species was classified according to the
terms defined below.
To assess whether sampling had any effect on the numbers
of rare species, the numbers of species recorded with just
one individual were counted in the individual samples, in
the pooled samples for the whole site and pooled across
14
the whole study area. The results were then graphed
against the number of samples.
localities are seriously undersampled to address the issue
of rarity and endemicity in the abyss.
Definition of terms
Taxonomy is also a potentially confounding factor, even
when the study was conducted by one group or
taxonomist. As a result it is not possible to amalgamate the
CCFZ 1 identifications with those from Kaplan as different
taxonomic teams carried out the identifications and there
has not been the opportunity to undertake an
intercalibration exercise. Damaged specimens and the
sheer number of species can make it difficult to maintain a
consistent taxonomy across many samples. To try to
mitigate against this, a conservative approach has been
taken in grouping the occurrence categories.
Common: Found in many samples across a site in relatively
high numbers (at least >5% in some samples) and also
found in all sites studied with similar site-relative
abundance.
Locally abundant and widespread: Found in some samples
within more than one site in abundance excess of 5% and
also found in other geographically separate sites.
Locally abundant widespread but rare in other localities:
Found in relatively high abundance (>5%) in samples at
one site but is also found in other sites but in much lower
abundance and maybe locally rare.
Locally rare but widespread: found in low numbers at any
one site but found in a number of geographically separate
sites.
Local widespread, rare and restricted: Found in a number
of samples across a site but in low abundance; not found
outside the site.
Rare: found only as single individuals in one or two
samples within a single site.
The relatively low number used for the percentage
abundance is a reflection of the generally low abundances
found in deep-sea systems. The exception being high
productivity areas associated with vents.
Caveats
Domes A samples were potentially compromised by poor
sorting and represent an impoverished estimate which
might account for the very low numbers recorded in this
site. The numbers of samples taken has a bearing on
species discovered but it is not a linear relationship so it is
difficult to be sure when the collectors curve would flatten
out. Domes A samples (47 Spade Box Cores) when
analysed indicated that between 30 samples would be
sufficient (Paterson et al. 1997). This means that the other
Results
Effect of sampling
There appears no obvious relationship between sampling
intensity and the number of species defined as rare (Fig.
3a). Restricting the analyses by removing the Domes A
data still shows that as expected there is high variation at
the single sample level which drops as more samples are
pooled (Fig. 3c). However, the current data suggest that
both the mean number and relative percentage of rare
species remains relatively high even when as many as 25
samples are pooled.
CCFZ. Rare species with only one occurrence in any sample
represented 48% of the total CCFZ fauna and if samples
with only occurring locally (potential endemics?) species
are included the proportion of the fauna restricted rises to
55% (Table 4). However it is interesting is that many of the
species found are locally rare but are found in sites across
the CCFZ sometimes they may be locally abundant (42.8%
of the total number of species). So this implies that such
species are in fact very widespread in occurrence and
occur at low densities. Increasing sampling may detect
more of such species but there is a diminishing return on
this in terms of effort.
A similar pattern can be seen in the EqPAC samples where
rare and locally endemic species comprise approximately
65% of the fauna. Similarly the widespread species
occurring in low numbers equate to approximately
34%.
Rarity appears to be a conspicuous and consistent
feature of the fauna of sediment habitats. Intensive
sampling points towards the discovery that single
occurrence species may actually be rare but have a
wide distribution either in the local area or across a
wider spatial extent. Despite this there remains a
significant proportion of species whose occurrence is
below the threshold of possible sampling intensity. It
is highly unlikely that such species are the sole
representatives remaining of their species given the
high numbers which are consistently found in
samples. Such a conclusion would imply either that
that the deep sea is populated, indeed dominated, by
species on the very brink of extinction; or that the
abyssal fauna represents a sink and that the viable
centre for the species is outside the abyss (Rex et al.
2005). However, with our current knowledge we are
unable to determine the likely distributions of such
species. Based on current data, the densities in the
CCFZ of such rare species would be below 1 individual
per 12.25 m2 based on samples taken across
distances of over 2700 kilometres. The nematode
data showed that there was a gradual reduction of
rare species as samples are pooled and a greater area
is sampled (Fig. 3d).
Magurran & Henderson (2003) consider that there are
actually two classes of occurrence – those species
which are fairly common and regular members of the
community and therefore consistently sampled and
those species which move in and out of the region and
can be considered as transient. This latter group can
appear rare but in fact may be widespread and
although locally in small numbers are relatively
abundant at a regional scale. The data presented
above would appear to endorse this perspective.
Figure 3a. Numbers of macrofaunal polychaetes recorded only in one
sample (rare species) from studies with different intensities of sampling
effort (number of samples). There appears to be no direct relationship
between the number of samples analysed and the tail of rare species
recorded, suggesting that rare species will always be a feature of deep-sea
samples. The data were derived from a number of abyssal studies.
Figure 3c. Percentage occurence of rare species does not appear to decrease
substantially as samples are pooled. At least 50% of the fauna is represented
by rare species.The Domes A samples removed from the analyses to avoid the
potential influence of the poor sorting.
Figure 3b. The polychaete samples analysed to test for the effect of
sampling on the numbers of rare species. As the samples are pooled as
expected the numbers of rare species decreases but it does not appear that
the decrease drops significantly with larger numbers of samples at the
regional scale.
Fig 3d. Percentage occurrence of rare species in nematodes from the
EqPAC transect shows a marked reduction as more samples are pooled.
But the number of rare species is still a high percentage when all the
samples are pooled.
15
Table 4. Results of rarity analyses
No. of
species
CCFZ
Rare
87
47.8
Locally widespread, rare and
restricted
13
7.1
Locally rare but widespread
64
35.2
Locally abundant widespread but
rare in other localities
7
3.8
Locally abundant and widespread
7
3.8
Common
4
2.2
182
100
Total number of species
No. of
polychaete
species
% of species
No. of
nematode
species
% of
species
101
59.3
70
34.3
9
5.3
28
13.7
55
32.4
95
46.6
Locally abundant and widespread
3
1.8
7
3.5
Common
2
1.2
4
2.0
170
100
204
100
EqPac sites
Rare
Locally widespread, rare and restricted
Locally rare but widespread
Total number of species
16
% of species
3. Study areas: current biogeographic knowledge and gaps
MIDAS has focussed on four main environments as part of the assessment of mining impacts: nodule province of the CCFZ, hydrothermal vents, non-active vents and non-vent hard substratum
environments, and methane hydrate zones in the Arctic and in the Black Sea. In this section an assessment of the current biogeographic knowledge of each these environments will be
presented. A case study is given to highlight some of the issues that we currently face in assessing in biogeographic studies. The main gaps associated with each area are also discussed.
3.1 CCFZ – sediment nodule fields
Figure 4. Map of the CCFZ showing contract areas and Areas of Particular Environmental Interest (APEI).(image ISA)
This region has been of interest since the 1970s and subject
to a number of studies (Mincks and Smith, 2006). Currently,
13 different contractors have exploration licences and are
undertaking a range of environmental studies in their
respective claim areas (Fig. 4). An extensive bibliography
has been accumulated for this region ranging from survey
reports (often grey literature) to comprehensive studies.
3.1.2 Physical and biogeochemical gradients in the
CCFZ
Deep-sea biogeographic patterns are frequently correlated
with large-scale biogeographic gradients [Lutz et al. 2010;
MacClain et al. 2012; Smith et al. 2008]. Within the CCFZ
there are two major biogeochemical gradients – an east to
west decrease in the nutrient flux to the ocean floor
(Wedding et al. 2013) and by a south to north decrease in
nutrient flux (Smith et al. 1996; 1997). C R Smith in a
presentation to the ISA proposed that the CCFZ could be
divided into nine regions, each with a different export
regime.
These gradients have an impact on the local abundance
and diversity of elements of the fauna, such that for
macrofauna there is a significant decline in their abundance
from east to west and from north to south (for example,
Glover et al. 2002; Paterson et al. 1997; Smith et al. 2008).
Large ocean basin cycles also impact on parts of the area, in
particular El Nino Southern Oscillation impinges the
southern edge of the CCFZ.
Productivity may affect recolonisation and recovery of
exploited areas. Studies of large-scale disturbances in the
deep sea returned conflicting results. The analyses of the
17
DISCOL area, following a simulated mining experiment,
indicated that the densities of motile megafauna had
returned to predisturbance values after three years.
Similarly, Glover et al (2001) found that polychaete
assemblages were still impoverished after decades in
turbidite-affected sediments off Madeira. Such a large-scale
disturbance can be considered as an analogue of a the kind
of disturbance which might result following mining. The
extent of the area disturbed coupled with overlying
production appeared to have an important effect on
recovery, but also depending on the fauna investigated (in
terms of size class, life history and functions).
Although studying disturbance at a much smaller scale,
Miljutin et al. (2011) investigated the recovery of nematode
assemblages following experimental test mining the CCFZ.
The nematode samples from tracks of the mining vehicle
were compared with nematode assemblages from
unaffected areas away for the test zone. After 26 years,
there were no signs of recovery neither in densities,
diversity nor composition (Miljutin et al . 2011).
3.1.3 Scales of habitat heterogeneity
Local topography is heterogeneous with differences in the
slope and nodule coverage at the km to 10s of metres scale
(e.g. Veillette et al. 2007). There are also large
topographical features such as abyssal hills through to
seamounts (Fig. 5). This means that to understand fully the
faunal composition of the region, the links and connectivity
both within and between areas within the CCFZ have to be
established as part of future sampling programmes.
Site
Position
Average annual
surface
productivity (gC
m–2 yr–1)
Certain elements of the fauna also provide
habitat for other organisms such as large
xenophyphores and komokiaceans. These
structural taxa respond to various
biogeophysical gradients and cycles and so
understanding the biogeography of the
structural taxa and what drives the observed
patterns will also help in understanding the
spatial distribution of associated taxa.
EQPAC 0°
0° N, 140° W
230
3.1.4 Molecular approaches
EQPAC 2° N
2° N, 140° W
200
EQPAC 5°
5° N, 140° W
155
EQPAC 9° N
?9° N, 140° W?
140
DOMES A
8° 27’ N,150° 47’ W
140
PRA
12° 57’ N,128° 19’ W
130
ECHO 1
14° 40’ N, 126° 25’ W
135
Molecular approaches, here defined as the
use of DNA sequence data, has great
potential in the analysis of biodiversity and
connectivity in areas of resource exploitation.
Molecular data have been used extensively in
recent years to address questions and
challenges in both marine and terrestrial
conservation science. These questions range
from the simple (e.g the identification of
species through DNA barcoding) to the
complex (e.g the analysis of the ecosystem
function and response of organisms through
study of their expressed genomes). The
technological progress of laboratory
Table 5. Surface productivity estimates from a number of sites across the CCFZ
(from Glover et al., 2002 based on Smith et al. 1997).
South to north gradient
West to east gradient
18
sequencing and computer analysis of DNA sequence data
has been extremely rapid, driven to a large extent by
biomedical, agricultural and forensic science. An example is
high-throughput sequencing (HTS), typically using
sequencing machines manufactured by the company
Illumina and now widely employed across almost all
biological sciences (Davey et al. 2011). These machines have
the potential to produce large reads of genomic DNA
sequences, at relatively low cost, from large numbers of
samples. However, a note of caution must be sounded:
blindly collecting large amounts of ‘data’ using HTS without
careful consideration of the scientific questions are being
addressed may not be the best approach to filling the gaps.
There are two main issues, firstly that of taxonomy and
secondly that of sampling bias. In both cases, molecular
data can in fact be the solution to the problem, but only
through careful and integrated workflow pipelines that link
new data to old.
Taxonomy, at its core a naming system that allows
biological data about organisms to be linked together, is
almost completely lacking in areas such as the CCFZ. This
means for example that contractors or researchers at
different sites in the CCFZ produce species lists that are not
comparable with each other, and that these species lists are
never transferred into formats that others can use (ie
named or described species linked to voucher material). For
example, despite over 130 scientific cruises to the CCFZ
since the 1970s (Nimmo et al. 2013), there is not a single
record of a polychaete (the dominant macrofaunal taxon)
on the Ocean Biogeographic Information System (OBIS)
within the 5 million square km area. In comparison, a
300,000 square km box drawn in the North Sea between
United Kingdom and Holland produces 95,000 polychaete
records on OBIS. The reason is that the North Sea has a well
worked taxonomy and useful field guides to the local fauna.
Molecular taxonomy can help, and in fact has the potential
to rapidly speed up this process. Firstly the description of
new taxa can be undertaken using DNA data as the primary
descriptive tool, alongside high-resolution imagery of key
morphological features (assisting identification at a later
stage). This sounds simple but requires a comprehensive
and fully-funded sampling-analysis-data-archiving pipeline
that starts with careful sampling and imagery, sequencing
of useful DNA markers and proper archiving of voucher and
type material in acessible museum or research collections
linked to online databases. The ‘speeding up’ of the
taxonomic process (Butcher et al. 2012) is enabled as the
DNA data takes away uncertainties with regard species
identity, and is easily archived on well-organised global
databases (NCBI GenBank). Molecular taxonomy does not
require HTS, but it does require a degree of morphological
data and proper archiving of voucher and type material.
Molecular taxonomy is not the same as DNA barcoding,
which in its typical definition is the identification of
organisms by sequencing a short DNA marker, such as
cytochrome oxidase I (COI) (Vogler & Monaghan 2007).
Molecular taxonomy is the creation of the reference
database that allows DNA barcoding to take place. In the
example of the CCZ, it is not currently possible to ‘DNA
barcode’ organisms from samples there because at present
there is no reference database to compare the sequences
with. It is possible, but unlikely, that matches will be made
from better studied regions (e.g bathyal depths or shallow
water) but recent surveys are showing that it is very rare
(Helena Wiklund, pers. comm.). A major effort must be
made to undertake quality molecular taxonomy from
poorly-known regions, the resulting database that will be
generated will allow future research and monitoring
programs to undertake rapid biodiversity assessment using
DNA barcoding.
DNA data has the potential for far more than the creation of
the basic, but essential, taxonomic database. The genomes
of organism contain a wealth of information on the
demographic history of the population to which it belongs
as well as the functional adaptation of the organism to its
environment. One of the more applicable with regard
deep-sea mining impacts is the estimation of migration
rates (e.g across the CCFZ or between hydrothermal vents)
and effective population size, which can be undertaken
from a surprisingly small sample size of just a handful of
individuals (Beerli & Felsenstein 1999). However, there is
debate as to whether this approach would be able to detect
intraspecific variation so more work needs to be done to
clarify this.
Today HTS approaches, with the enormous amounts of
genetic data from just single individuals, and the
sequencing across whole genomes in non-model organisms
(NMOs) allow this to be undertaken using analysis of just
one or two individuals.
functional response of that organism to environmental
stress or variable.
Of these approaches, all of them potentially of great
benefit, those most likely to be applied to questions of
biodiversity and connectivity in deep-sea mining regions in
the near future are probably (2) RAD-seq and (4) eDNA. The
RAD-seq approach can be applied to the study of population
genetics, with questions such as migration rates, gene flow,
and effective population size being of direct relevance to
management decisions. There are examples of RAD-seq
being used in population studies in aquatic organisms (e.g
Keller et al. 2012), but rather few to date in the deep-sea,
(although see Pante et al. 2014). A recent study of
HTS approaches on NMOs can currently be split into five
major categories (Willette et al. 2014): (1) Whole Genome
Sequencing (WGS) i.e the sequencing of entire genomes
and assembly using reference
transcriptomes, (2) RAD-seq, i.e the
Figure 5. Seafloor image showing seafloor topology in the eastern German Claim area
sequencing of a large and
of the CCFZ. The brown features representing seamounts of varying elevations and
randomized sub-sample of shorter
sizes. There are a large number of such features within the area. Knowledge of the
fauna associated with some of these features would be useful to place the species in
homologous regions of the genome
the mining areas into a biogeographic context. (Image from BGR)
using restriction enzymes, (3) the
Amplicon method, i.e the
enrichment (using PCR) of a large
number of genetic regions of
interest (or markers) across whole
genomes typically thousands of
single-copy genes/exons for the
study of phylogenetics, (4) the
metagenomic approach, or more
commonly ‘environmental DNA or
eDNA’ method in which a large
number of sequence reads from
environmental samples (e.g mud or
seawater) are assembled into
operational taxonomic units (OTUs)
which are assumed to be species
and can be analysed as such across
samples or regions of interest and
(5) RNA-seq (or gene expression
study) which is a fairly rapid way of
investigation which genes are being
expressed in an organism or group
of organisms and as such the
19
foraminifera in the Southern Ocean deep-sea has revealed
the potential utility for rapid assessment of potential
biodiversity in eDNA samples (Lejzerowicz et al 2014).
Sampling bias, an age-old problem in deep-sea studies, does
not disappear with the advent of HTS. RAD-seq approaches,
even with decreasing costs in the future, are unlikely to
applied to anything other than abundant and
well-characterised species such as charismatic vent fauna.
eDNA has great potential to provide long-lists of OTUs for
microbial and protists species, but there is currently no
knowledge of the spatial scale of sampling required to take
eDNA samples of larger metazoa. Careful, academic
research must be undertaken on these biases and the
appropriate sampling scales required before these HTS tools
become widely used by contractors involved in EIA
assessment.
3.1.5 Patterns of biodiversity in the CCFZ
Current Knowledge: Biogeography of major faunal groups
Megafauna
Tilot (2006) has provided an overview of the current
knowledge of megafaunal abundance, diversity and
biogeography. However most of the information in her
report is restricted to a few sites within the CCFZ, especially
the French claim areas. Data are lacking on the distribution
of megafauna from other claim areas. A workshop on
megafauna was held in 2013 at Wilhelmshaven, Germany
which brought taxonomic experts and contractors together.
A review of the morphotypes of various key groups,
holothurians, sponges, fish, etc. was undertaken. An atlas of
these morphotypes is available (http://ccfzatlas.com). In
addition a series of recommendations was made to the ISA.
The main one being that specimens were desperately
needed to provide good taxonomic resolution, images and
video were not enough. Current knowledge is restricted to a
number of scientific publications, which are often old (>30
years) and in need of updating and revision. Nevertheless,
the taxonomy of certain megafaunal taxa is quite well
20
established, i.e. echinoderms, fish, some cnidarians, while
others need much more work, i.e. sponges and protistans.
Meiofaunal biodiversity
Yet, to date, studies in both nematodes and harparcticoids
have been conducted at various taxonomic levels (species,
generic and family), which greatly hampers intercalibration
of data sets (e.g,, Miljutin et al. 2011, Ahnert & Schriever,
2001, Vopel & Thiel 2001). Furthermore many families of,
for example, harparcticoid copepods had been revised in
recent years making comparison with historical data sets,
such as DISCOL (Ahnert & Schriever, 2001) even more
challenging (P. Martinez, pers. communication). To date
there have not been any molecular study examining the
diversity and connectivity of meiofauna across the CCFZ.
There are a number of studies dealing with the meiofauna
from the Pacific polymetallic nodule area, e.g. Hessler and
Jumars 1974; Snider et al. 1984; Mullineaux 1987;
Renaud-Mornant and Gourbault 1990; Bussau et al. 1995;
Radziejewska and Modlitba 1999; Ahnert and Schriever
2001; Radziewska et al. 2001a,b; Radziejewska 2002;
Lambshead et al. 2003; Miljutina et al. 2010 and Miljutin et
al. 2011. Radziejewska (2014) presented the most recent
Microbial biodiversity
update on meiobenthos from the Central Pacific nodule
province. So far investigations of meiofaunal biodiversity in
Protista. Protistan communities from the CCFZ are mostly
the CCFZ have mainly focused on harpacticoid copepods
known from Foraminifera. This group is abundant in
and nematodes, which typically represent the most
samples and is thought to play a substantial role in carbon
dominant meiofaunal taxa in the abyss. Though other
cycling. Larger protistans, like xenophyophores may also
higher taxa, such as ostracods, kinorhynchs, tardigrades,
provide habitat for other eukaryotic organisms (Lecroq et al
gastrotrichs, and acari are also present (Radziejewska
2009). Abyssal Foraminifera morphotypes have been
2014). Analyses of nematode assemblages revealed
studied extensively, for example Gooday et al. (2004);
between 10 and 246 nematode genera per study with most
Schröder et al. (1988).
occurring throughout the CCFZ. However, differences in
generic composition between the eastern CCFZ and the
Some of the hard-shelled morphospecies recorded in
central part of the CCZ have been reported (Radziejewska et
Kaplan samples from the Eastern and Central CCFZ by
al. 2001, Miljutina et al. 2010); the nematode genera
Gooday et al. in Smith et al. (2008) were widely distributed
Terschellingia, Desmoscolex and Pareudesmoscolex seem to
in the Pacific and other oceans, such as Adercotryma
be more prevalent in the eastern CCFZ whereas
glomeratum, Spiroplectammina biformis, Lagenammina
Thalassmonhystera, Theristus and Acantholaimus are more
tubulata, L. difflugiformisand and some of the Reophax
dominant in the central part.
morphotypes (e.g. R. helenae, ‘R. bilocularis’ and ‘R.
scorpiurus’). The widely distributed species, however,
Between 34 and 62 genera of harpacticoid copepods are
represented a small proportion (approximately 7%) of the
known from the CCFZ (Radziejewska, 2014). Harpacticoids
species recognised at the Kaplan sites.
(species, generic and family level) have been used to
monitor faunal responses following experimental and test
Many of Gooday et al. (2004)’s monothaumous
mining in the CCFZ and DISCOL area (Ahnert & Schriever,
morphotypes were also recorded widely in more than one
2001, Radziejewska et al. 2001a, Mahatma 2009; Miljutin et
ocean basic, i.e. Atlantic and Pacific, and more than one
al. 2011). For example, species diversity and the total
locality within the Pacific. Nozawa et al. (2006) studied
density of harpacticoids recovered after 26 years following
sediment Foraminifera from one site in the eastern CCFZ
an experimental test mining study in the CCZ, whereas
and reported that some of the morphotypes of
species composition had not returned to pre-mining
Foraminifera and komokiacean were similar to those with a
conditions (Mahatma 2009).
wide distribution, recorded from other ocean basins.
Nevertheless, several other morphotypes had a more
Macrofauna – Case Study 2
It is important when analysing biogeographic patterns to
understand whether the fauna changes because of
turnover – the replacement of one species group with
another – or whether the fauna appears to be a restricted
subset of the overall species pool – nestedness. It is
important that these two aspects of b-diversity are
separated or at least their contributions to the
measurement is detailed, as very different conclusions
and therefore management decisions can be made. For
example, nestedness implies that the fauna is
fundamentally one species pool and that activity, which
might cause an effect in one area, is unlikely to impact the
pool generally. However if faunal turnover is the primary
finding activity in one area could have profound impacts
on the fauna.
In the CCFZ it has already been established that there are
both east – west and north – south gradients (Table 5)
and so it is hypothesised that such gradients will structure
the biogeography of the benthic fauna. In other deep-sea
studies the impact of productivity gradients has led to
both nestedness in the case of molluscs – particularly
gastropods (Brault et al. 2012) but also turnover –
asteroids (Brault et al. 2013). So it appears that different
taxa will respond in different ways to potential gradients.
In this section the response of macrofaunal polychaetes
will be tested using archived data from a number of
studies in the CCFZ. The reduction in nutrient transport
across the CCFZ may well result in a reduction in the
similarity of the fauna. It is reasonable to hypothesise
that such a gradient may well lead to nestedness. “Put
Spionid polychaete from the CCFZ
with an apparent widespread
distribution (NHM)
simply, as POC-flux decreases … species drop out because
of insufficient food supply.” (Brault et al. 2013).
The first based on a comparison across the CCFZ
undertaken by George Wilson (Australian Museum;
Paterson et al. 1997). The second was an analysis of
polychaetes from the EqPac programme (Glover et al.
2002). A third dataset made during the Kaplan study
(Smith et al. 2008) also studied sites from the east to west
of the CCFZ. Unfortunately none can be amalgamated
because of differences in the taxonomy; each was
identified by a different set of taxonomists. In both
samples sets there were a high number of new species
and so classification was to a numbered OTU. These OTUs
have not yet been intercalibrated. A fourth data set
looked at meiofaunal nematodes identified from the
EqPac transect (Brown, 1998; Brown et al. 2000). While
this taxa is not strickly macrofauna they are included to
indicate the generality of the patterns obtained.
Methodology
The analyses of b-diversity follows the approach outlined
by Baselga (2010). The methodology proposed provides a
more robust separation of the contributions of
nestedness and turnover to the dissimilarity between
sites than previous methods, i.e. NODF (Almeida-Neto et
al., 2008). Analyses was undertaken using the R scripts
provided by Baselga (2010) – beta-multi.R and
beta-pairwise.R (R Development Core Team, 2006). The
analyses are based on presence-absence of species.
rather that different species area able to survive at
different points along the gradient.
Results
However these results are based on low numbers of sites
and /or sampling within a site. Only DOMES A had
sufficient sampling for the species accumulation curve to
approach asymptote. This means that effectively each
site could be a random subset of the regional species
pool, the lack of nestedness notwithstanding. This is
because of the large ‘tail’ of rare, apparently site-unique,
species encountered at all sites sampled. Sufficient
sampling will never be achievable so detecting the real
distribution of these species will remain problematical.
Nevertheless the implication for assessing environmental
impacts in the CCFZ is that consistent sampling across the
area, together with unified taxonomy is essential. While it
may not be possible to sample adequately to solve the
problem of the ‘rare endemics’, a stratified and
comprehensive sampling programme will go someway to
providing the data that can be used to support
management.
CCFZ east to west indicates that overall dissimilarity Beta
SOR is =51% but that there is virtually no nestedness (B
NES = 0.02) while the turnover component is relatively
high (B SIM = 0.49). There are several dominant species
shared across the CCFZ which underlie the overall
similarity and possible contribute to the nestedness
value.
The EqPac north–south gradient shows a slightly modified
pattern with higher overall dissimilarity (B Sor=0.78) but
again indicates that it is turnover (B Sim = 0.63) not
nestedness (B NES = 0.16) which accounts for the pattern
in polychaetes. For the nematodes, a similar high level of
dissimilarity is observed and also turn-over which appears
to be responsible for the patterns observed (BNES =
0.1.7).
Overall the results point to degrees of faunal turnover
with distance as postulated by Paterson et al. (1997) and
Smith et al. (2008).. The biogeographic analyses points to
a relatively large number of species common across the
CCFZ, both east to west and north to south but with a
varying number of unique species at each site. It does not
appear that the nutrient gradients found in the CCFZ drive
nestedness of the fauna as might have been predicted,
Table 6. b-diversity measures for the CCFZ stations based on polychaetes – PRA, ECHO and
DOMES A; Polychaetes and Nematodes–EqPac 0N, 2N, 5N, 9N and HOT station 23N, Kaplan
polychaetes. SIM=Simpson’s multiple site dissimilarity; SOR = Sorensen’s pairwise dissimilarity
measure of turnover, NES = nestedness measure.
$beta.SOR
dissimilarity
(spatial turnover)
$beta.SIM
â-diversity
$beta.NES (nestedness)
Polychaetes multi.ccz
0.511
0.487
0.0244
Polychaetes Kaplan
0.806
0.625
0.181
Polychaetes multi.eqpa
0.783
0.626
0.156
Nematodes EqPac
0.629
0.460
0.168
Image of the head of the
nematode Acantholaimus
angustus from the CCFZ
(Senkenberg)
21
Table 7. Summarising the bacterial and archaea composition found in
COMRA area A (Xu et al. 2005).
The majority of the clones isolated had a high (95%) similarity to
other environmental clones from other regions
Bacterial composition
46 clones (RLFP)
32 species 27
genera (16SrDNA)
Proteobacteria
i. Gammaproteobacteria
ii. Alphaproteobacteria
iii. Theta/deltaproteobacteria
75%
92.9%
5.3%
1.8%
Non-sulphur bacteria
5.3%
Cytophaga-Flexbacter-Bacteroides
11.8%
Unclassified
5.3%
Archaea composition
Marine group 1 - Crenarcheota
22 clones
restricted distribution within the Pacific e.g. Resigella
moniliforme, or within the CCFZ region. Nozawa et al.
(2006) stress the need to re-examine the original material.
There were at least 10 species of foraminifera that are
abundant at one of the three Kaplan sites, but rare or
absent at the other.
Molecular analyses of Foraminifera has revealed
considerable diversity, much of it not yet related to
morphotypes and thought to reside in the small size
fraction of benthos (Lecroq et al. 2009ab;2011; Pawlowski
et al. 2011). New discoveries are likely to increase with
greater sampling. These analyses indicate that most of the
deep-sea sediments are undersampled with regards to this
taxon. Yet despite this high biodiversity, molecular evidence
suggests that for at least some species, biogeographic
distributions may be quite large and interoceanic (Lecroq et
al. 2009).
22
In general though, Foraminifera show similar
biogeographic patterns to other elements of the benthic
assemblages, some apparent cosmopolitan species,
those with a more ocean basin distribution and then
those with restricted distributions. The data suggests
that significant turnover of major components of the
foraminiferan faunal over scales of roughly 1,000 km
across the CCZ. More sampling is needed to provide a
better understanding of the distribution of this group at
a number of different spatial scales.
form biofilms and so may be particularly associated with
nodules and their formation (see section below).
Virtually nothing is known about other protistan taxa
such as ciliates, flagellates etc. The importance of this
obvious gap in knowledge is also unknown.
Xu et al. (2005) reported that the majority of the bacteria
isolated were Proteobacteria (Table 7) and that the majority
appeared to be similar (>95%) to isolates from other
environments. Many proteobacteria are metal-reducers. It
is perhaps not surprising that such types of bacteria are
commonly distributed and recorded from habitats such as
vents. The Cytophaa- Flexbacter- Bacteroides group showed
a higher degree of novelty with only 61-93% showing a
degree of similarity with other environmental clones, but
again many isolates appeared related to those from a very
wide range of habitats. The implications from Xu et al.
Bacteria. Bacterial communities are thought to be
important foundations for the nutrient cycling and
related ecosystem services. In nodule areas microbial
communities, particularly bacteria, also play a role in
metal cycling and may be involved with nodule
formation (Xu et al. 2005; Wang et al. 2010). Some of the
isolates belonging to the Pseudomonas are known to
Studies of such communities are not yet common in the
CCFZ (Wang et al. 2010, Wu et al. 2013; Xu et al. 2005; 2007
see Tables 7 and 8) but some patterns can be deduced.
Bacterial communities are often diverse and show similar
taxon richness and community patterns as other elements
of the fauna such as macrofauna, e.g. high diversity with
long tails of unique or rare taxa.
Table 8. Results from Wang et al. (2010). Four sites across the central Pacific, the first three within the CCFZ, the fourth
outside the Area and close to the continental slope of Mexico.
Station
Depth
No of
sequences
isolated
No of
OTUs
Dominant group
West WS0505
Highest nodule concentration
5120 m
68
47
Alphaproteobacteria
Deltaproteobacteria
East ES0502
5307 m
63
58
Gammaproteobacteria
Alphaproteobacteria
East ES2005-01
Lowest nodule concentration
5197 m
67
45
Gammaproteobacteria
Alphaproteobacteria
ES2005-03
Lowest concentrations of MnO and
Fe2O3
4299 m
115
71
Alphaproteobacteria
Deltaproteobacteria
(2005) are that the microflora from the nodule province is
composed of representatives closely related to widespread
clones. Molecular sampling methodologies have improved
and so has the resolution. However, molecular sampling
methodologies have improved and so has the resolution.
The low numbers both of samples and of isolates cautions
against reading too much into these early results.
In a comparative study of four sites across the CCFZ, Wang
et al. (2010) found a similar bacterial composition to Xu et
al. (2005). The Proteobacteria were the dominant group
within which Alphaproteobacteria (23.3%) and the
Gammaproteobacteria (21.7%) were the most abundant of
the isolated sequences. The dominant non-Proteobacteria
group was Acidobacteria – 7% of the total sequences.
Betaproteobacteria, Chloroflexi, Firmicutes,
Verrucomicrobia, were minor with <3% of the
sequences.
Wang et al. (2010) showed that in terms of
biogeography the bacterioflora had similarities with
other faunal groups. While many isolates are
restricted, approximately half showed basin-scale
distributions, being closely related to isolates from
areas of ocean crust, the Pacific nodule province and
marine basalts; some CCFZ isolates were very similar
to clones from these habitats (=99%). The marine
basalts and crusts contain large amounts of Fe and Mn
and are highly reactive. Wang et al. (2010) suggest
that the similarity is related to bacterial function particularly
manganese oxidising abilities.
Within the CCFZ, there were also differences in the occurrence
of particular microbial groups pointing to potential basin-scale
biogeographic patterns possibly related to the presence of
nodules and their densities. At the level of the isolate, similar
patterns to other fauna were observed with some being
restricted to one site while others occurred across the CCFZ, or
across more than one site. In this latter finding bacterial
biogeographic patterns bares some similarity to other elements
of the fauna.
A polychaete species belonging to the genus Parexogone.
This species reproduces by developing stolons along the
body which then grow into miniture versions of the adult
and break off to lead separate lives. The stolons can be
seen in the picture as outgrowths coming off the body.
Image: A.Glover (NHM) and Viacheslav Melnik
(Yuhzmorgeologia)
23
3.1.5 CCFZ: Nodule fauna
Mining will remove nodules. Yet the nodules are
themselves a habitat or series of microhabitats which are
utilized by a range of organisms (Mullineaux 1987; Theil et
al 1993; Veillette et al 2007). Our knowledge of the nodule
fauna is remarkably scarce considering the amount of
study that has been directed towards them. Previous
studies have been mostly geological and mineralogical
with little focus on the organisms using the nodules as a
substratum or potentially as a substrate. Nodules are one
of the few hard surface habitats in the abyss and therefore
potentially have a different species composition to the
surrounding sediment. The importance of these organisms,
particularly the bacteria, is that they may be agents in the
formation nodules and accumulation and cycling of metals
within them (Lysyuk, 2011; Reiman, 1983; Wang et al.
2009 and references therein).
Megafauna. Many taxa appear to use nodules as a
potential hard surface upon which to settle and grow.
Images taken from the region indicate large protistans,
sponges, cnidarians such as actiniarians and octocorals,
crinoids, particularly stalked taxa, and ascidians are
observed on nodules. Megafaunal organisms often have a
large geographic range and photographs do indicate some
widespread morphotypes (http://ccfzatals.com). Images
cannot totally resolve the taxonomy of the megafauna.
More studies based on collected specimens are needed
and so it remains difficult to be sure of the distribution and
biogeography of large epifaunal taxa. The lack of
specimens means that there is no information as to
whether the morphotypes observed are opportunistic or
obligate nodule epifauna. Similarly if species are not
obligate then might they occur on other hard surfaces such
as rocky outcrops on spreading centres or on seamounts?
Macrofauna. Mullineaux (1987) compared the macrofauna
from nodules in two sites in the Pacific, one within the
CCFZ (Domes C), and with samples from metallic crusts on
a seamount (Table 9). There was a high degree of
‘endemism’ in that most of the taxa recovered were
restricted to one nodule site (71%), with only one species
24
Table 9. Macrofauna recovered from nodules and crusts (from Mullineaux, 1987).
Taxon
No of
species
Distribution
Functional Group
Sponge
5
4 species nodule only
1 species nodules and
crusts
Suspension feeder
Cnidaria: Hydrozoa
4
3 species nodules only
1 species crusts only
Suspension feeder
Cnidaria: Scyphozoa
1
Nodules and crusts
Cnidaria: Anthozoa
2
Nodules only
Suspension feeder
Annelida: Polychaeta
3
morphotyp
es
1 species nodules only
1 species crusts and
nodules
1 species crusts only
Deposit and suspension
feeders
Mollusca: Gastropoda
3
Nodules only
Deposit feders
Mollusca: Bivalvia
2
Nodules only
Suspension/deposit feeders
Mollusca: Mono and
Polyplacophoran
2
Nodules only
Deposit feeders
Crustacea: harpacticoid
1
Nodules only
Deposit feeder
Crustacea: Tanaidacea
1
Nodules only
Deposit feeder
Bryozoa
8
7 species nodules only
1 species crusts only
Suspension feeders
Brachiopoda
1
Nodule only
Suspension feeder
Echinodermata:
Crinoidea
1
Nodule only
Suspension feeder
Tunicata: Ascidiacea
2
Nodule only
Suspension feeder
being found in all sites and a further one being recorded
from the crusts and one of the nodule sites. Four species
were common to the two nodule sites (11%). It must be
stressed that this was a restricted study and that a greater
sampling both of nodules and metallic crusts is need.
Mullineaux concluded that a major driver for the species
richness was nutrient availability particularly nutrient flux
from the surface.
Thiel et al. (1993) studied the epifauna associated with
nodules and detected that there were distinct
microhabitats such as crevices between and within nodules
which were inhabited by a distinct fauna. Little is known
about the spatial distribution of such epifauna assemblages
at a basin scale or between ocean basins or whether such
fauna also occur in metallic crusts on seamounts.
Protistan assemblages. Mullineaux (1987) found 64 species
of Foraminifera on nodules, the dominant group. Table 10
shows the numbers of species recorded from sites and
between sites. While many species appeared to occur
across the sediment sites of the Eastern North Pacific and
Central North Pacific, the fauna found on the crusts were
not found in the nodule sites. Mullineaux noted that there
was little overlap between the nodule fauna and species
found in the sediment. She found that the abundance and
percentage cover of many Foraminifera suggested that they
may also be important agents in nodule formation.
Veillette et al. (2007) studied four nodule zones, three
within the French eastern and one in the western CCFZ site
(Table 11). Each zone had a different nodule facies with
different sizes and coverage of nodules. The aim of the
study was to assess whether there were distinctive
microhabitats within the nodules and whether there was a
distinct associated fauna with them.
The vast majority of foraminiferal morphotypes (85%) were
widespread across the two sites and also across the
different facies identified. This contrasted with the
macrofauna species which appeared more endemic
recorded from only one facies of the eastern region (59%).
In terms of local diversity, the eastern
sites were more species rich than the
west, possibly a measure of the higher
nutrient flux in the east. They also noted
that exposed nodule surface was a
significant factor in determining the
number of species found on nodules at
a regional scale. They concluded that
the greater the range of microhabitats,
i.e. nodule surface complexity, the
greater the habitat heterogeneity and
therefore more species diversity.
Veillette et al. (2007) noted an overlap
with Mullineaux (1987) species, 21 of
the 73 species they recorded similar to
those of Mullineaux.
Caution needs to be exercised in
interpreting these results. The study
relies on morphotypes. Molecular
analyses on Foraminifera have returned
equivocal results with some species
appearing to be widespread but many
apparently more restricted, possibly
endemic. Further work is needed
focused on reconciling morphotypes
with a molecular barcode (Pawlowski et
al. 2013) but also which extends the
sampling to provide a more rigorous
survey across the CCFZ. As with the
epifaunal macrofauna, these studies
also need to look at the relationship of
the fauna associated with polmetallic
cobalt-rich crusts and nodules.
Table 10. Foraminifera species recorded by Mullineaux (1987) from a number of sites in
the Pacific. Crusts is a site of metallic crusts on the Hawaiian Islands chain, the other
areas are nodule zones, ENP is within the CCFZ, CNP is outside the Area.
No of
species
Eastern
N Pacific
Cen
tal
N
Paci
fic
Cru
sts
Crusts
+
ENP/C
NP
ENP &
CNP
ALL
19
2
12
5
16
8
Table 11.Spatial distribution of fauna found on nodules based on Veillette et al. (2007).
Two sites were sampled – one in the East with three different nodule facies and one in
the West with just one facies.
Both
East and
West
All E
facies
Two
E
facies
One
East
facie
W only
Foraminifera
morphotypes
61
1
3
5
2
Macrofauna
3
4
10
Microbial Assemblages. Wu et al. (2013)
compared the bacterial assemblages of
metallic nodules from two sediment
sites in the CCFZ and from the flanks of
a seamount (Table 12). In addition they
compared the diversity and composition
of bacteria on nodules and in the
25
sediment. The diversity of bacteria as determined from 16S
rRNA sequences was high with 1013 bacterial sequences
representing 414 OTUs and with 640 sequences
representing 31 Archaea MOTUs. While there was a degree
Table 12. Degree of specificity between nodules and the
sediment for the bacteria based on Wu et al. (2013)
Nodules
Only
Both
Sediment
only
Bacteria
189
55
170
Archaea
10
12
9
of overlap between the nodule assemblages and the
sediment, each habitat had a distinctive assemblage (Table
12). Wu et al. (2013) reported that the bacteria appeared to
be more diverse in the sediments at two sites but at the
Table 13. Bacteria and Archaea community composition from
sediments and nodules
15 phylogenetic bacterial groups unique to nodules
Gammaproteobacteria
57 OTUs
Alphaproteobacteria
41 OTUs
Deltaproteobacteria
37 OTUs C
Closely
related to
vent OTUs
implying
metal cycling
functionality
155 phylogenetic bacterial groups unique to sediment
Deltaproteobacteria
26
44 OTUs
Many related
to bacteria
from various
marine
sediments
third there was no difference, indicating a degree of
heterogeneity. But they also reported that the rarer
bacterial groups were found on the nodules perhaps a
suggestion that the nodules have specific assemblages. The
Archaea had a higher diversity on the nodules that from the
sediment and overall had a lower diversity compared to the
bacteria.
on seamounts, and nodules. More work across all the size
categories is needed to establish the degree of
commonality as these areas beyond the easily exploitable
seafloor may harbour the same species and thus act as a
reservoir either for subsequent recolonisation or for future
conservation.
3.1.6 CCFZ: Gaps to our knowledge
In terms of assemblages the composition differed between
sediment and nodules (see Table 13). The members of each Sampling and sampling methodology
assemblage appeared to have close similarities to bacteria
There is a lack of standardisation in both the sampling
from other marine environments; the nodule bacterial OTUs
programmes and the methodology. Despite decades of
more closely to those from vents and other metal rich
exploration few data have been made available in the
environments while the sediment OTUs to other marine
scientific literature. These datasets are a mix of academic
sediments.
research cruises, i.e. JGOFS, and environmental cruises by
contractors, i.e. KORDI, IOM (see Mincks and Smith, 2006).
Comparison of the fauna between the three study sites
The latter data may be available to the ISA but are not
showed a similar pattern for both the bacteria and archaea,
generally available to the wider scientific community.
the nodule assemblages from one of the CCFZ sites
(WS0904) and from the flank of the seamount clustered
together and all the sediment sites clustered as a group.
This suggests that the sediment assemblage was comprised
of widely distributed OTUs while the nodule assemblages
had more distinct and restricted assemblages (Wu et al.
2013). They concluded that microhabitats were more
important than distance between localities and that
similarities between the bacterial assemblages had more to
do with functional aspects, particularly metal cycling, than
with biogeography.
As with the other faunal studies caution must be taken in
interpreting these results because of the lack of sampling
across a range of scales. However, the association of some
isolates with nodules and their hypothesised role in nodule
and mineral cycling needs further investigation. In
particular are these isolates only found on nodules or are
they do they have a more diverse metabolic repertoire?
The answer could have important implications for
exploitation and the role of APEIs.
Tantalizing preliminary evidence suggests that for some of
the taxa there may be links between metallic crusts, found
Such a gap in data availability makes any assessment of the
distribution and biogeography of fauna difficult. However
even the release of data will only be of limited value
because there is little intercalibration of the taxonomy
between the contractors and even between the academic
studies. This is because many of the species being
discovered are new to science and the formal taxonomic
classification of these new taxa lags far behind the
environmental studies.
Large-scale geographic coverage
The central and north-eastern areas of CCFZ are without
data. Claim areas are undersampled. There are no data
available for the APEIs. Nor is there any incentive or
regulatory imperative for any of the contractors to
undertake surveys in such areas. So there is no way of
knowing how representative these areas might be.
Sampling standardisation and effectiveness for
biogeographic and connectivity studies
Different sampling gears collect different elements of the
fauna. Quantitative devices such as box cores generally
provide good samples in nodule areas but they suffer from
the drawback that the macrofaunal infauna is sparse so
considerable sampling is required to adequately sample the
environment. This results in considerable effort to process
the resultant cores to isolate specimens. Quantitative
meiofaunal samplers such as multicorers are faster and
provide larger numbers of individuals but identification of
the meiofauna can be problematic – even of a molecular
approach is employed. Next Generation Sequencing and
omic (genomic, transcriptomic and proteomic) approaches
may provide a solution but the costs in terms of processing
samples and the informatics involved mean that this
approach is, at the moment, still beyond standard
monitoring methodologies.
Qualitative samplers such as epibenthic sledges are able to
provide enough specimens of macrofauna and smaller
megafauna. The fact that they are not quantitative is not a
drawback for biogeographic studies. Again combining this
gear with molecular and morphological study can provide
data useful to connectivity (i.e. population genetic studies)
and biogeography. Some of the contractors are now using
this approach. The disadvantage to this is that epibenthic
sledges, like other sampling devices, may be selective in the
organisms and size classes they capture.
Different contractors undertake megafaunal surveys in
different ways, over different amounts of surface area,
using a variety of gears from video sledges to ROVs and
submersibles. The results of a workshop in 2013 on
megafauna from the CCFZ indicated that imaging was
insufficient for the kind of taxonomic resolution required to
assess biogeographic distribution of key megafaunal
species.
Existing Data and Access
Currently we lack data on faunal distributions across a
range of scales from local to regional. Given the
heterogeneity present across the region again at a range of
scales this makes it particularly difficult to assess
connectivity and patterns of biogeography of the fauna.
Similarly, different faunal elements, from micro to
megafauna, are likely to demonstrate different patterns of
distribution across the abyssal regions. Contractors follow
the regulations and guidelines as laid down by the ISA and
are collecting data, very little of it is available to either other
contractors or to the scientific community.
Taxonomic impediment
Much has been made of the taxonomic impediment in
deep-sea biodiversity research. There are a number of
reasons for the lack of formal taxonomic study of the
samples already available but the consequence is a lack of
data just at a time when the need is crucial. The ISA has
recognised this and is convening a series of workshops to
try to standardise taxonomy between contractors.
The main issue in developing a biogeographical overview of
data being collected by the contractors for the ISA is that
there is no taxonomic consistency between the contractors.
The nature of the contracts for exploration does not
encourage or require any collaboration between
contractors. All contractors are required to undertake is
environmental assessments of their own areas and submit
these data to the ISA. Therefore, when assessment of
potential impact are being addressed it is actually
impossible for any contractor to be able to say with any
degree of certainty that exploitation of the mineral
resources will not have irreversible consequences, such as
the extinction of species, because there are not the data to
be able to compare species between areas. The ISA is the
obvious organization to enable this comparison to be made
by making data available from the contractors. But
consistent taxonomy of all groups is lacking to enable these
fundamental analyses to be undertaken. This obvious failing
has been recognized the Legal and Technical Commission of
the ISA. A number of taxonomic standardization workshops
is being organized to address the lack of data.
Taxonomic standardisation is compounded by a lack of
expertise–some contractors do not have access to trained
staff and there is generally a lack of taxonomic experts to
aid with training or undertake the identification and
standardisation of the fauna. This lack is often not just the
lack of a suitable taxonomist but the lack of time available
for existing experts to be able to work on samples from the
CCFZ. Some areas such as the Protista also have shortages
in expertise.
The microbial area is also neglected and in this case it is a
result of the regulations not requiring microbial
assessments of the benthic environment to be undertaken.
For the megafauna few samples of individual specimens are
available and as a result there is little genetic information.
Fauna on nodules
Is it distinct? Significantly different from surrounding
sediment? If so how? Are their specific obligate
relationships or is it facultative and opportunistic?
For example, sponges are a dominant element of the
megafauna. How many images of sponges show them
associated with nodules? We do not yet know if the same
sponge species are to be found in areason seamounts as
well as the nodule areas. In nematodes there seems to be a
difference between the species found in nodules crevices
and those found in the sediments surrounding nodules
(Thiel et al. 1993). There will need to be further research to
assess whether these differences rise from different
abundance levels of faunal assemblages, or if nodules and
sediment clearly host different sets of species and genera.
Microbial communities form biofilms on nodules and are
thought to be involved in nodule formation and manganese
oxidation but it is not clear whether this relationship is
obligate and preliminary evidence suggests that many
bacteria and archaea may be shared across metal-rich
habitats.
Nodule fauna relationship to fauna on hard substratum
habitats on seamounts within claim areas and across the
region generally needs to be investigated.
27
Molecular sampling
Megafauna
Taxonomy
Advances in molecular techniques may provide
a faster and more pragmatic approach.
Currently, a major disadvantage of most
methods is that they do not provide estimates
of abundance of the organisms being isolated.
And even here new approaches in
transcriptomics will enable future studies to
undertake a full molecular assessment. The
pace of technological advance in this field of
analyses and interpretation suggests that some
form of molecular methodology will become
routine in general ecological research.
However, for the current contracts such
methods have not been widely used and are
unlikely to become routine in the short term.
KNOWLEDGE GRID for CCFZ
Sampling
The lack of molecular data, given modern
taxonomic practice, is particularly limiting in
addressing the issues of species distribution
and biogeography. Increasingly survey teams
are turning to molecular methods to provide
quick taxonomic results (A.Glover, pers.
comm.) But there is still a need to provide such
data to enable comparisons between contract
areas and thus provide the biogeographic
patterns needed to assess potential impacts of
exploitation.
Meiofauna
Microbial:
Protista
Microbial
Bacteria
Microbial
Archaea
Taxonomic
resolution
Good general
knowledge of
species
But wide use of
morphotypes
reduces resolution
Limited to a
few taxa.
Mostly
(M)OTU
Limited to a few
taxa Mostly
(M)OTU. Some
taxa only to family
or genus level
Foraminifera and
Xenophypohores.
Many (M)OTU
Limited
MOTU
Limited
MOTU
Keys, etc
Available for many
groups but may be
in need of revision
Available for
some groups
None available
None
N/a
N/a
Taxonomic
information
availability
Some exchange of
information
between scientists
No
intercalibration
No
intercalibration
Mostly academic
exchange
Data available
via external
databases
such as
GenBank
Data available
via external
databases
such as
GenBank
Sampling
Mostly video and
still imaging
Quantitative
and qualitative
samples
Quantitative
samples
Quantitative
Quantitative
Quantitative
Molecular
sampling
Little
Limited
Limited
Some
All molecular
- eDNA
All molecular eDNA
For video and stills
but not for
specimens.
Collecting gear
used is based
on ISA
recommendatio
ns but new gear
being
introduced –
epibenthic
sledges
ISA have
recommendations
which apply
Limited but
follows accepted
scientific standards
Limited but
follows
accepted
scientific
standards
Limited but
follows
accepted
scientific
standards
Some but
scattered in
scientific literature.
Spatial coverage
insufficient
Some but
scattered in
scientific
literature.
Spatial coverage
insufficient
Assessment for
some groups –
Harpacticoids
Spatial coverage
insufficient
Some preliminary
assessments but
coverage limited
Some but
limited to a
few areas
Some but
limited to a
few areas
Consistent
sampling
between
different teams
Biogeogrphic data
28
Macrofauna
3.2 SMS – MIDAS areas from the Mid Atlantic Ridge
The Mid-Atlantic Ridge (MAR) in the North Atlantic is a semi-continuous, complex series of rocky ridges, fracture zones, seamounts and areas of volcanism. The ridge is an active spreading
centre with a central rift valley. Features such as sediment fields found in areas between rock ridges and outcrops represent 95% of the MAR. The combination of habitats contributes to
environmental heterogeneity on a range of scales (Priede et al, 2013).
The MAR separates the east and west
Atlantic basins potentially acting as a
barrier to distributions but has also
been hypothesized as a pathway and
stepping stones for the distribution of
fauna. The circulation of water
masses within the Atlantic is affected
by the MAR and deep interchange
between the two main basins is
complex often being focused on
particular features such as fracture
zones (Lackschewitz et al. 1996).
a
b
Differences in overlying production
have been noted along the ridge, for
example, the northern areas
overlying the Reykjanes Ridge to the
north of the Sub-Polar Front have
been shown to have a higher
productivity than areas to the south
(Gebruk et al. 2010). However, the
presence of the ridge itself is not
thought to enhance overlying
productivity although shallower
Figure 6 a) ISA map showing the two claim sites on the MAR. b) MAR around the Azores EEZ, TAG and Snakepit occur within the French claim
features associated with the ridge,
area while Logachev occurs in the Russian claim area (IMAR).
e.g. seamounts, may produce
localized areas of increased
production and are often associated
MAR (Bergstad et al. 2008; Bergstad & Gebruk, 2008) and
(Braga Henriques et al, 2012, Tempera et al. 2010) and
with deep ocean fisheries (Preide et al. 2013b; Braga
UK-led MAR-ECO (Priede et al. 2013a) provided the most
sponges aggregations (Tempera et al. 2010).
Henriques et al, 2013)
recent studies on the MAR outside the Azores EEZ (Fig. 6b).
All of these studies report that the high heterogeneity and
The MAR is a slow spreading ridge system. The active
In general studies on the MAR have been few or particularly
undersampling greatly underestimate the biodiversity of
volcanism associated with the spreading centres along the
localized as in the case of hydrothermal sites with sustained
the MAR. The Azores Triple Junction area is also
MAR has resulted in a series of hydrothermal vent sites.
studies based around the Azores EEZ. Expeditions led by
characerised by a high density of non-hydrothermal
These are generally widely separated, 100–350km apart
Russian oceanographers (Mironov & Gebruk, 2006)
habitats often dominated by deep-water coral communities
(Murton et al. 1994; German et al. 1996). Van Dover (1995)
together with large European multidisciplinary studies ECO
29
suggested that the larger distances between active areas
was relatively large and thus might act as a biogeographic
filter.
At the species level, the some of the larger megafauna
Pacific Rise vents (Cuvelier et al. 2014, Gollner et al. 2010b).
species have been studied to assess population
12 dirivultid copepods are currently described from MAR
connectivity, e.g. the vent mussel Bathymodiolus (Comtet
vents and 4 species even occur in other oceans (i.e. Pacific)
et al. 2000; O’Mullan et al. 2001; van der Heijden et al.
(Gollner et al. 2010a). A first molecular study on dirivultids
Despite some biogeographic studies on vent megafauna
2012) and its symbionts (Won et al. 2003; Duperron et al,
showed that this taxon might have high dispersal potential
using genus data at the global scale, little has been
2006), the blind shrimp Rimicaris (Teixeira et al. 2011; 2012)
(Gollner et al. 2011).
conducted on different vents from the Mid-Atlantic Ridge.
and associated bacteria for some vent fields (Petersen et al.
Microbial biodiversity
The lists of species lists were published in the 90’s and early
2010), Riftia pachypila at the population level (Shank and
2000’s (Van Dover et al, 1996; Desbruyères et al, 2001;
Halinych 2007). Such studies have also compared
Protistan. There are few studies of protists around vents.
Cuvelier et al. 2011), have just been recently updated, but
populations from the two biogeographic provinces
Folliculinid foaminifera were found in large numbers on
no clear quantitative data, and often with no supporting
proposed by Bachraty et al. (2009) – 8ATJ and North
settlement panels sited in Clam Acres on the East Pacific
genetics analyses.
Atlantic.
Rise site (Van Dover et al. 1985) which implied that
Macrofaunal biodiversity
foraminiferans were likely to be found and that some
Vent fauna is evolutionarily adapted to the hydrothermal
species may be common. No studies have been undertaken
chemosynthetic ecosystem. It is highly specialised and often
Macrofaunal studies are not numerous. The mussel bed
on the MAR.
endemic to a particular vent system (Van Dover, 2012). As a
fauna of Logatchev, Snake Pit and Lucky Strike were
result the biota is particularly at risk should active vent sites
Bacterial
compared by Van Dover and Doerries (2005). They found
be mined.
that there was evidence of a north-south split in the faunas,
Bacterial biota associated with vents encompass both
partly explained by depth, Lucky Strike is shallower than the
The vents TAG, Snakepit and Logatchev are currently being
free-living and symbiotic species. There is evidence that
two
southern
sites,
but
also
by
geological
setting
at
the
evaluated by contractors from France and Russia as
some symbiotic species also occur as free-living. There are
sites. All three sites had many of the same species but with
potential areas for the mining of massive sulphide deposits
just a few studies on the biodiversity or functional
different abundance and could be differentiated as a result.
(MSD) (see Fig. 6b). Some of these sites have been studied
biodiversity of microbes (Creapeau et al. 2011).
since 1988.
Meiofaunal biodiversity
3.2.1 Patterns of biogeography
Megafaunal biodiversity
The large charismatic megafauna are one of the visual
characteristics of vent sites. Different vents often having
different suites of these organisms. For example, many sites
in the Atlantic are characterized by immense swarms of
shrimps such as Ramicaris, while those of the Galapagos
vents have mixtures of large clams and tube worms.
Biogeographic studies depend on the number of vent fields
explored, the methods and the underlying hypotheses used
to delineate them. This has resulted in the North Atlantic
being considered either as one biogeographic province
(Bachraty et al. 2009; Moalic et al. 2012) or as two (Van
Dover et al. 2002).
30
3.2.2 MAR-Vent systems: Gaps to our knowledge
Meiofaunal diversity and biogeography is rather poorly
studied at the MAR. Diversity is likely relatively low, with i.e. Sampling and sampling methodology
15 meiofauna species found associated with mussel beds at
German et al. (2011), in summarising the next phase of
Snake Pit (Zekely et al. 2006a), and ~20 species found
research after the Census of Marine Life, estimated that
associated with artificial substrates at Lucky Strike (Cuvelier
only 20% of global mid-ocean ridges have been investigated
et al. 2014). Most dominant taxa are dirivultid copepods, a
and they calculated that as many as 1000 vents were yet to
family which is endemic to the vent environment (Gollner et
be discovered. It can be assumed that some of these will be
al. 2010a), harpacticoid copepods and nematodes which
on the MAR. In the recommendations for future work,
both are represented by genera known from a variety of
biogeography stands as a recurrent area of research for all
other environments. Whilst only a single nematode species
the hydrothermal regions. They also highlight the MAR is
from MAR is taxonomically described (Zekely et al. 2006b),
one of the regions in need of more research. The critical
the knowledge on harpacticoid copepod species is a bit
questions which remain to be answered focus on the
better: Smacigastes micheli (Ivanenko et al. 2004, 2012,
discovery and assessment of the distribution of the biota
Cuvelier et al. 2014) was reported several times from Lucky
associated with vents systems. It is clear that many gaps
Strike, Bathylaophonte azorica was reported from Snake Pit
remain even in this relatively well-studied ecosystem (for a
and Lucky Strike (Zekely et al. 2006 a, Cuvelier et al. 2014),
deep-sea habitat).
and Xylora bathyalis was found at MAR vents and on East
Large-scale geographic coverage
As suggested above considerably more vents are thought to
exist. Within the MAR system more surveys will provide
sites between the known ones. This should provide more
data on the distribution of key species.
Sampling standardisation and effectiveness for
biogeographic and connectivity studies
connectivity. As commercial exploration activities increase
the ISA (2004) have put forward standardised protocols
which contractors are expected to follow. There is,
however, no such agreement between research teams.
Existing Data and Access
Existing data are mostly within scientific literature, lab
research reports, students’ theses. Generally available.
Data are not widely available from later commercial
exploration of the two claim areas
Different teams tend to study vents for a range of reasons
and even multidisciplinary studies tend to have a range of
objectives. As a result standardised approaches to
surveying, sampling and subsequent analyses are difficult.
This generates a lag between the initial results and data
which can be standardised for biogeographic and
Taxonomic impediment
The charismatic nature of the large megafaunal organisms
are usually well covered, although the lag between
discovery and formal classification can still be quite long. As
for other habitats, classification of the smaller biota often
lags behind the sampling. As pointed out by Van Dover
(2012) the rate of discovery of macrofaunal vent species
shows no sign of levelling off even in well-studied sites.
Taxonomic resources are not adequate to provide the
necessary data quickly, and possibly not within the
timeframe between exploration and exploitation unless
better taxonomic pipelines are established.
Molecular sampling
Sampling for genetic analyses is now becoming a
standardized approach. Some taxa lack any genetic data but
these are becoming the exception. There are good
protocols and standards now in place.
3.3 Non-active vents and non-vent hard substratum sites
3.3.1 Current Knowledge: Biogeography of major faunal
groups
Megafaunal biodiversity.
Outside the direct influence of the vent fluids (inactive
areas and the beyond vent fields), there are significant gaps
in our knowledge, not only due to the lack of data, but also
due to the patchiness of the habitats. Despite the North
Atlantic being the best studied oceanic basin concerning
deep-water benthic organisms (Cairns, 2007; Mironov &
Gebruk 2006; Watling & Auster 2005), even in this region,
data on the distribution of many megafaunal organisms is
still scarce. This lack of information may result from: 1) the
absence of sampling in most deep-sea areas because of
high costs and technological challenges; 2) difficulties with
identification of the species sampled or in collections; or 3)
they may simply be naturally rare across their distribution
range.
The mega and larger macrofauna of the MAR have been
assessed in a number of recent studies. Sampling in MAR is
challenging and undersampling remains an issue. MAR ECO
studied the region to the north of the Azores. Table 14
summarises the distribution patterns of the taxonomic
groups reported. Most of the taxa have wide geographic
ranges with the morphotypes being found in other areas of
the Atlantic or extending into other oceans.
The results from the MAR-ECO project indicate that despite
decades of sampling new megafaunal species are still being
discovered. From a relative low number of trawls one new
genus of echinoid, four new species of holothurian, four of
ophiuroids and one new asteroid species were discovered.
Macrofauna
Little is known, of fauna of the sponge aggregations and
coral gardens and coral framework. There are some recent
data from the Condor seamount in the Azores (Bongiorni et
al. 2013, Zeppilli et al. 2013) but with no supporting
molecular data information. For example, within the group
of epizoan zoanthids associated with octocorals, most
information available in the Atlantic Ocean comes from
shallow water, but recent studies have revealed the
existence of an hidden diversity in the deep-sea with the
identification of several new genera and species
(Carreiro-Silva et al. 2011; Carreiro-Silva et al in prep).
The macrofauna associated with the sediment found
between ridges along the MAR were studied by Shields and
Blanco-Perez (2013). They reported that the MAR did not
appear to present a physical barrier to the distribution of
macrofauna and that the diversity was similar to the
continental margins are comparable depths. However, with
a few notable exceptions, most of the species were
identified to morphological OTUs and so links of this MAR
fauna to the continental margins or abyssal plains remains
unknown.
Meiofauna
Very few papers have been produced comparing hard
surfaces with other environments or between seamounts
and surrounding sediments. In a recent paper Zepilli et al.
(2013) reported urgent research was needed on this topic.
31
KNOWLEDGE GRID for MID ATLANTIC RIDGE - Vent systems
Meiofauna
Microbial:
Protista
Microbial
Bacteria
Microbial
Archaea
Good general
knowledge of
species
Generally good
resolution
Limited to a
few taxa
(M)OUT
common
Limited
MOTU – both
free-living and
symbiotic
MOTU
Keys, etc
Available for many
groups.
Monographic
treatment/fieldguide
Available for
some groups
None
None
N/a
N/a
Taxonomic
information
availability
Scientific literature,
on-line databases
Scientific
literature,
on-line
databases
Limited
information
?
Data available via
databases such as
GenBank
Data
available via
databases
such as
GenBank
Sampling
Quantitative ad
qualitative; video
surveys
Quantitative
and qualitative
samples
Quantitative
samples
Quantiitative
Quantitative
Quantiative
Molecular sampling
Almost standard
Becoming
common
Becoming
common
?
All molecular eDNA
All molecular
- eDNA
Consistent sampling
between different
teams
Widespread
acceptance of
sampling
methodology
Widespread
acceptance of
sampling
methodology
Widespread
acceptance of
sampling
methodology
?
Limited but
follows accepted
scientific
standards
Limited but
follows
accepted
scientific
standards
Sythensis available
but more spatial
coverage would be
useful.
Some but
scattered in
scientific
literature.
Lacking
sufficient spatial
coverage
Assessment for
some groups –
Harpacticoids
but others
lacking sufficient
spatial
coverage?
Some.
Coverage?
Biogeographic data
32
Macrofauna
Taxonomic
resolution
Sampling
Taxonomy
Megafauna
Some .
Coverage?
3.3.2 MAR – non-vent and off vent environments: Gaps
to knowledge
Sampling and sampling methodology
The heterogeneity of the environment make standardised
approaches difficult – different types of trawl and
semi-quantitative gears are used. Similarly differences in
the sampling programme and strategies using ROV and
AUVs between different research and contracting teams
make existing data held by institutes available. To some
extent this is being done but specimen records in Museums
and other institutes are often not available. Releasing this
data or digitising such records would provide another
source of information about species level biogeography.
The heterogeneity of the MAR non-vent sites is a major
challenge to collecting. Traditional methods
using quantitative samplers such as corers
Table 14. The number of species collected during the MAR-ECO project and an assessment of their
are very difficult to deploy successfully.
biogeographical distribution. The numbers in the body of the table represent the number of species of each
Semi-quantitative methods such as trawls
taxonomic group.
have been used in projects such as
Also in
MAR-ECO and ECO-MAR but such gears only
NW
MAR only
N. Atlantic
NE Atlantic
other
Atlantic
collect megafauna and often the condition
oceans
of the samples are poor.
Hexactinellida1
ROVs are frequently deployed in rock areas
and can provide valuable specimens and
quantitative samples but the numbers of
ROVs are limited, the areas surveyed and
sampled can be quite small compared with
the size of the environment and navigating
among the complex topography
encountered can be challenging.
Nevertheless they represent to optimum
way to sample the smaller elements of the
biota. Carefully planned sampling strategies
together with extensive collecting are
probably the optimum way to provide the
data on species distributions along the MAR.
Large-scale geographic coverage
Anthozoa2
Hexacorallia
Antipatharia
Scleractinia
Octocorallia
Echinodermata
Asteroidea3
Ophiuroidea4
Holothuroidea5
Echinoidea6
7
1
3
2
1
1
3
4
1
1
2
4
3
16
14
5
4
1
2
1
1
1
4
6
7
6
Taxonomic coverage is problematic as
mentioned above.
Molecular sampling
Considerably more molecular samples
need to be collected as part of
sampling programmes. Larger
specimens need to have molecular
subsamples taken. The specimens need
to be imaged both in situ (if taken by
ROV) and ‘on deck’. Sediment samples
need to be processed on ship and the
infauna imaged, subsampled for
molecular analyses or if large enough
fragments taken and frozen or
preserved in absolute ethanol for
future analyses.
1
Microbiology
Tabachnick & Collins (2008); 2 Molodtsova et al. (2008); 3 Dilman (2008); 4 Martynov & Litvinova (2008); 5
Gebruk (2008); 6 Mironov (2008)
1
There are gaps in the coverage along the
MAR and particularly off-vent areas. Historical records tend
to be concentrated around the fishing areas such as
seamounts around the Azores (see Moldosova, 2007; Braga
Henriques et al. 2013 for a review).
Sampling standardisation and effectiveness for
biogeographic and connectivity studies
3
Taxonomic impediment
make standardisation difficult. There are various examples
of best practice which could be adopted if agreement on
over all data needs was made.
Protista. Very little is known about
protistan diversity from hard surfaces
as they are difficult to sample. No
published data could be retrieved.
Bacteria and Archaea. No literature sources were found for
this biota.
Existing Data and Access
Historical data is being collated for some regions such as the
Azores but more ‘data archaeology’ could be carried out to
33
Cnidarian megafauna–Case study 3
The current knowledge of the taxonomic diversity and
distribution patterns of octocorals is scarce and
fragmented, compounded by the lack of taxonomic
expertise (Riedel et al, 2013]. The North Atlantic Ocean is
one of the most comprehensively studied regions
(Watling & Auster, 2005; Cairns, 2007), For example,
knowledge on octocoral taxonomy is not uniform on both
sides of the Atlantic. Most recent octocoral taxonomic
studies have focused on the northwestern Atlantic (Gulf
of Mexico, Florida Strait), resulting in the description of
several new species [e.g. Quattrini et al, 2014]. By
contrast, the octocoral fauna of the northeastern Atlantic
(Mid Atlantic Ridge, Porcupine Seabight, Rockall Trough),
and Mediterranean (e.g. Alboran Sea, Silicily Channel)
have received less attention, with most taxonomic
inventories dating back to the early 1990’s (Grasshoff,
1986; Vafidis et al. 1994). Moldosova (2008) suggested
that the Mar-Eco data 40.6% of the fauna was widely
distributed beyond the Atlantic (see Table 14). In the
Central Atlantic (Azores), a recent study has identified
164 species in seamounts and island slopes, but there
were a large number of octocorals with uncertain
taxonomic affinity (Braga Henriques et al, 2013).
Underlying factors influencing the regional distribution
are complex and have not been clearly identified for the
MAR. There are both latitudinal and bathymetric patterns
in the corals around the Azores (Braga Henriques, 2013).
The majority of records were concentrated in 100–600 m.
Factors such as hard substratum availability, hydrography
and productivity were hypothesised to play a part. The
highest diversity found coincided with important fishing
areas suggesting that both habitat availability and
productivity are central to local to regional distributions.
Modelling of coral distributions using similar approaches
to Titttensor et al. (2009) around the Azores and along
the MAR may be useful in developing predictions as to
the impact of mining MSD off-vent areas.
Most of the studies that have been done on the
reef-building coral Lophelia pertusa (Le Goff-Vitry et al,
2004) have focused on the northern seas around Norway
and Scotland. Some genetic population studies have been
done comparing the northern fjords with the east Atlantic
offshore areas. It was shown that there was a high
genetic differentiation between fjord subpopulations and
offshore ones. For this species associated microorganism
have also been subject of recent studies showing that
coral skeleton surface, coral mucus, ambient seawater
and reef sediments present clear habitat-specific
differences in community structure and species richness
based on operational taxonomic unit (OTU) numbers on
the Norwegian communities (Schöttner et al, 2009). To
the best of our knowledge the few studies of beta
diversity for this species have been done on populations
from western Scotland (Henry et al. 2009).
There is little information on the distribution at the global
scale of the octocoral genera Corallium (Sampaio et al,
2009). Corallium is best known as species exploited to
provide jewelry but only certain species have a
commercial value. Most Corallium species live in
restricted geographical areas. The Western and Central
Pacific (from Japan to northern Philippines and Hawaii)
and the Northeast Atlantic are hotspots for these
gorgonians (Sampaio et al, 2009). Corallium rubrum
Lamarck, 1816 in the Mediterranean and other seven
species from the Western Pacific and Hawaii form large
aggregations in the upper bathyal (to 500 m) and support
local fisheries.
amphiatlantic C. niobe Bayer, 1964 and C. medea Bayer,
1964, which is restricted to the American slopes. In this
context, the Macaronesian deep-sea rocky bottoms
emerge as a probable radiation centre for these species.
As for other cold water corals, Corallium spp. are highly
sensitive to anthropogenic disturbances: they have slow
growth rates, relatively late maturity, long life spans, and
limited dispersal potential).
A better understanding of the factors which underlie the
distribution of species of Corallium is needed together
with surveys to determine how common it is in different
areas associated with off-vent mineral sites.
Outside this subtropical belt, there are records from off
Ireland and the Bay of Biscay ( Grasshoff 1982b, 1986).
Apparently, these species do not aggregate, are
uncommon throughout the area, and their biology is
virtually unknown. In the western Atlantic the genus is
less diversified, and according to Watling & Auster (2005)
only two species are known from that region: the
Octocorals and scleratinians from the MAR.Left: Colony of Corallium tricolor from Menez Gwen marine protected area. Middle: Dense colonies of Madrepora oculata and Lophelia pertusa
with a rockfish. Right: Trachyscorpia cristata echinata. (Images courtesy of IMAR/DOP)
34
KNOWLEDGE GRID for MID-ATLANTIC RIDGE - Non-vent environments
Sampling
Taxonomy
Megafauna
Macrofauna
Meiofauna
Microbial
Protista
Microbial
Bacteria
Microbial
Archaea
Taxonomic
resolution
Good general
knowledge of
species
Generally good resolution
but OTUs from sediment
regions
Limited to a
few taxa
(M)OTUs
common
Limited
MOTU –
MOTU
Keys, etc
Available for many
groups.
Monographic
treatments for
some taxa
Available for some groups
None
None
N/a
N/a
Taxonomic
information
availability
Scientific literature,
on-line databases
for some taxa
Scientific literature, on-line
databases
Limited
information
?
Limited
information
Limited
information
Sampling
Quantitative, video
surveys
Quantitative and
qualitative samples
Quantitative
samples
Limited
samples
available
Limited
Limited
Molecular
sampling
Limited
Becoming common
Becoming
common
?
All molecular
- eDNA
All molecular
- eDNA
Consistent
sampling
between different
teams
Sampling variable
between studies
Widespread acceptance of
sampling methodology
Widespread
acceptance of
sampling
methodology
Limited but
follows
accepted
scientific
standards
Limited but
follows
accepted
scientific
standards
Some synthesis for
some taxa but
spatial coverage
variable - most
information from
northern MAR
Some but scattered in
scientific literature. Lacking
spatial coverage
Insufficient
coverage
Insufficient
coverage
Insufficient
coverage
Biogeographic data
Insufficient
coverage?
35
3.4 Methane hydrate – Svalbard margin and Black Sea
3.4.1 Svalbard margin.
These seep sites have only recently been discovered so
there is relatively little biological information available (e.g.
dos Santos et al. 2009), most of the reports focused on the
geological setting (e.g. Bunz et al. 2012). While initial
surveys indicated that sites along the Svalbard margin are
likely to be similar to those on the Norwegian margin and
the well-studied Håkon Mosby mud volcano site, seep sites
do have faunistic differences (Vanreusel et al. 2009). Such
differences relate to the oceanographic, geochemical
settings and the depth of the seep. As a result there is a
limited amount of detailed biogeographical assessment that
can be made at this point. The priority for future research
should be to undertake general survey which will place this
region into context with the other areas within the Arctic.
36
Figure 7 below images of gas hydrate fields from the west of Salbard (78°35’N, 9°40‘E) and from the Håkon Mosby Mud Volcano
Left. At a water depth of 380m off western Svalbard – the upper limit of the gas hydrate stability zone in the area – methane is released and seeps from the
seafloor. The methane itself or sulfide generated upon the anaerobic oxidation of methane (AOM) in the sediments fuels biomass production by chemosynthetic
microorganism. Gutless siboglinid tubeworms hosting chemoautotrophic symbionts appear in dense colonies and are partly covered by filamentous sulfide
oxidizing bacteria. Other members of the benthic community depicted in the image include sea spiders and bivalves. Expedition HE387 of the German RV HEINCKE,
August/September 2012. Image courtesy of MARUM – Center for Marine Environmental Sciences, University of Bremen, Germany.
Midle. At a water depth of 380m off western Svalbard – the upper limit of the gas hydrate stability zone in the area – methane is released and seeps from the
seafloor. The methane itself or sulfide generated upon the anaerobic oxidation of methane (AOM) in the sediments fuels biomass production by chemosynthetic
microorganism. Gutless siboglinid tubeworms hosting chemoautotrophic symbionts colonizes soft sediments between boulders and cobble stones next to whitish
mats of sulfide oxidizing bacteria. Anemones and gadid fish are also visible in the image. Expedition HE387 of the German RV HEINCKE, August/September 2012.
Image courtesy of MARUM – Center for Marine Environmental Sciences, University of Bremen, Germany.
Top right. A sea spider living on methane-rich muds emitted from the subsurface at the Håkon Mosby Mud Volcano (HMMV) at 1250m water depth. Expedition
ARKXXIV/2 of the German RV POLARSTERN, July 2009. Image courtesy of MARUM – Center for Marine Environmental Sciences, University of Bremen, Germany.
Bottom right. Muds and fluids with high concentrations of methane from deep subsurface reservoirs are emitted at the Håkon Mosby Mud Volcano (HMMV) at
1250m water depth. Whitish mats of thiotrophic bacteria that oxidize sulfide generated by anaerobic oxidation of methane in the sediments appear at the surface.
It appears that also non-seep organisms, e.g., zoarcid fish and starfish benefit from this chemosynthetic primary productivity. Expedition ARKXXIV/2 of the German
KNOWLEDGE GRID for SVALBARD MARGIN
Megafauna
Taxonomy
Meiofauna
Microbial
: Protista
Microbial
Bacteria
Microbial
Archaea
Mostly
dominant
species ,
MOTU and
OTU
MOTUs
MOTUs
N/a
N/a
Resolution to
species possible
Resolution to
species possible
Resolution at
family and
genus level is
good but
species is poor
Keys, etc
Some available
Russian keys to
many groups.
Other primary
works and keys to
particular taxa
available
Family and
genus level.
Few species
level
Taxonomic
information
availability
Good
background
knowledge of
Arctic Megafauna
species available
Good background
knowledge of
Arctic macrofauna
species. But new
species possible
Mostly primary
sources
Mostly
primary
sources
Gene
sequences
on external
databases
Gene
sequences
on external
databases
Sampling
Specimens
needed as well as
video/still imaging
Quantitative and
qualitative at
different spatial
scales needed
Quantitative at
different spatial
scales
Quantitative
at different
spatial scales
Quantitative
at different
spatial scales
Quantitative
at different
spatial scales
Molecular
sampling
Essential
Essential
Essential
Essential
Essential
Essential
Good
background
available to place
sites into context
of Arctic
biogeograph
Increasing
information to
produce
contextual
information
Synthesis is
needed based
on more
taxonomic
work
More
needed
More
needed
More
needed
Taxonomic
resolution
Sampling
Macrofauna
Biogeographic
data
Little
available
37
3.4.2 Black Sea
The deep zones of the Black Sea are unique in the World Ocean
in that they are totally anoxic below 100 to 200 m. The Deep
Water Mass is the domain of anaerobic processes dominated
by bacteria and archaea (Kuypers et al. 2003; Durisch-Kaiser et
al. 2005). Surveys of the microbial systems were undertaken
during the EU HERMES project (Foucher et al. 2009). A large
range of microbial communities was analysed. The discovery of
carbonate reefs indicates some of the unique aspects of this
deep-sea system (Arnds et al. 2007). Microbial diversity was
heterogeneous in the reefs with different parts having distinct
diversities. The Archaea involved in this process were
anaerobic methane oxidising groups but sulphur-reducing
bacteria were also present. There also did not seem to be any
consistency in community composition between the reefs;
each being a mixture of the main species. A great deal more
study of this remarkable ecosystem is needed.
Microbial biogeography as it relates to ecosystem functioning is
a priority. What are the connections between the sulphur and
methane reducers in this system with those found in vents and
Figure 9 (left and right) Carbonates formed upon anaerobic
oxidation of methane (AOM) by consortia of sulfate reducing
bacteria and archaea build large reef structures at 220m depth
at the northwestern Crimean shelf. While the microbial
communities fueled by gas seepage from the seafloor form
extremely high biomasses within the up to four meter high
chimney structures, any metazoan life is missing due to the
absence of oxygen in Black Sea waters at this depth.
Expedition M72/2 of the German RV METEOR, March 2007.
Images courtesy of MARUM – Center for Marine
Environmental Sciences, University of Bremen, Germany.
41
seeps? Generally, microbial biogeography depends on the
sampling. Various assessments indicate that several isolates
have wide distributions. How much this is a result of limited
taxon sampling remains to be determined. All ecosystems
studied indicate that isolates with wide distributions are the
result of functional congruence rather than biogeography.
4. Modelling
The logistical difficulties, expense and vast areas associated
with deep-sea sampling leads to gap in the knowledge of
faunal distribution. One approach to fill these gaps on the
spatial distribution of species is the species distribution
model (SDM). This approach correlates species occurrence
(presence-only or presence–absence) records with
environmental data in geographic space to explain and
predict a species’ distribution. A wide variety of SDM
methods have now been developed, including correlative
and mechanistic approaches. Each approach has advantages
and disadvantages, but the vast majority of studies to date
have been correlative.
Such models were first applied in the terrestrial domain
where their use has increased rapidly over the past 20 years
and is now applied in conservation biogeography. By
comparison, application of SDMs to marine species is rare,
although interest in their application is increasing. Their use
has been recently advocated in the support of marine
spatial planning .
In the deep sea, SDMs are increasingly used but mainly to
predict the distribution of Cold Water Corals (CWC) . The
emphasis given to CWC can be explained by three main
reasons: i) they are recognized as vulnerable, threatened or
ecologically significant by a number of regional or
international agreements ; ii) taxonomy is consistent and
presence data are widely available in open-access
databases and iii) environmental data that best explain their
occurrences such as temperature, aragonite saturation
state, primary productivity or bathymetry and its derivatives
are available at global scale . The resolution of the
environmental dataset however is a major restriction to the
reliability and applicability of cold water coral SDMs. The
first global scale models to be developed had a resolution of
about 100 km. The best predictors for CWC occurrences
were temperatures, oxygen, aragonite saturation state and
enhanced primary productivity thus providing a global
envelope for potential environmental niches. Regional to
local scale models now have a resolution on the order of 10
m or even less . In these models, bathymetric terrain
attributes have shown good potential as environmental
predictors as they act as proxies indicating areas of
enhanced currents and food supply for suspension-feeding
corals , narrowing down the footprint of the potential niche.
In the framework of the environmental management of
resource exploitation in the deep sea, SDMs such as those
developed for CWC may prove useful to fill gaps in the
distribution of megafaunal assemblages associated with
inactive vents or cobalt crusts as these environments are
potentially suitable for sessile suspension feeders including
CWC. The reliability of such models would be constrained
by the availability of data on the occurrence of species in
the area to be modeled as well as the resolution of the
bathymetry. Indeed, SDMs have proven powerful when
they are used for interpolation (i.e. to fill in the
geographical gaps in species distribution within an area
where occurrences are known) but the most commonly
used correlative SDMs are limited in their ability to
extrapolate species distribution across space or time . For
example, modeling the distribution of species along the
mostly unknown southern Mid-Atlantic Ridge should not
rely on correlative models developed from the better
known northern Mid-Atlantic Ridge. Modeling the
distribution of species in nodule provinces would further
face three major issues: i) taxonomically robust datasets are
limited for most taxonomic groups and nodule provinces; ii)
SDMs would only apply to the most common and
widespread species but not the bulk of rare species for
which no correlation with environmental factors could be
drawn; and iii) the environmental drivers for species
distribution are not well constrained nor are the influence
of functional traits such as dispersal ability or the
phylogeography of species. These later biotic drivers of
species distribution are not considered in correlative
models but the development of processus-based or
mechanistic approaches coupled with correlative models
are promising tools.
Species distribution models are thus valuable tools to fill
gaps in the known distribution of species, which are
increasingly used in conservation biogeography. As any
model they may provide insights into the most critical gaps
in knowledge that need to be filled through targeted studies
and as any model their reliability is highly constrained by
the quality and resolution of input data, both biological and
environmental.
5. General discussion
The known
The information gained by over a century of research and
discovery has produced data on the identification and
distribution of many large megafaunal organisms. The
revelation of high species diversity in the deep-sea
sediments has been verified across the World Ocean. While
the discovery of chemosynthetic systems with their
associated large, abundant megafauna has resulted in
focused study and exploration of such systems. In
chemosynthetic systems taxonomic knowledge has almost
been able to keep up with the discovery of new vents and
seeps. The factors driving the local and to some extent the
regional distribution patterns have been established. But
for the other high diversity environments and for the
smaller sized biota taxonomic and biogeographic knowledge
have not been able to keep pace with the rate of discovery
or sampling. The drivers of local and regional diversity
42
patterns have been hypothesised but a robust ecological
framework is still being developed.
The unknown
contractors and research groups. However, time is short
and the resources being deployed are not always
commensurate with the effort needed. Providing sufficient
resources is important to concentrate effort on the key gaps
needed to be filled before irretrievable change occurs.
Despite considerable sampling in the deep sea over the past
century, our knowledge of the distribution of organisms at
To fully understand the faunal composition of the region,
different scales is rudimentary. Certainly, very few areas
the links and connectivity both within and between areas
have been studied sufficiently to be able to assert with any
within potential mining areas have to be established as part
degree of confidence what the impact of mining will be on
of future sampling programmes.
the survival of species. The scale of the problem is mirrored
by the vast size of the environment. Yet there is an
The unknowable
opportunity to address many of the key questions by
focussed biological sampling programmes, use of new
Deep-sea sediment samples are characterised by a long tail
genetic technologies and greater collaboration between
of species with only one or possibly two individuals which
have not been recorded from other sites and often found in
a single sample. Quantitative samples are particularly
conspicuous in this regard. The presence of rare species
appears to be an emergent property of deep-sea systems
and is not just a function of sampling efficiency. It is
therefore unlikely that we will ever be able to know the
distribution of these species and whether they are in
danger of extinction due to mining and mineral extraction.
Modelling, improved genetic sampling and co-ordinated,
nested sampling programmes may go some way to reducing
the risk but such approaches will not totally solve this
problem. Ultimately it will be to policy makers and
regulators to make the decision as to allow exploitation.
6. Conclusions
We have been studying the deep-sea ecosystem for over a
century and in that time have made significant advances in
our understanding of the fauna and ecology of this part of
the planet. Yet the knowledge we have is not enough to be
able to predict, let alone guess, what the long-term
consequences of extracting mineral resources will be. There
are several reasons which explain our apparent ignorance
despite all the efforts that have been made to explore and
explain this ecosystem. The most obvious one is the sheer
scale of the ecosystem itself. Efforts to date have only
literally scratched the surface of a very small area. It is also
a difficult environment to sample, requiring good
technologically-advanced, ocean-going vessels to deploy
scientists and collecting gear. Thus sampling programmes
tend to be focussed and of limited duration. The kinds of
surveys which were common in the early days of deep-sea
43
research and championed by the Soviet programmes of the
1950s and 60s are no longer fundable. Collections of biota
are therefore usually from surveys of particular areas to
address particular scientific questions. Sample coverage is
as a result very patchy and subsequently it is difficult to
make extrapolations from such small sample sets. This
change in focus is a reflection of the way science is funded
and carried out. The consequence for biogeographic studies
has been that taxonomy, the description and classification
of species, has become more difficult to fund. There have
been exceptions in recent years associated with the novelty
of seep and vent species but the numbers involved are
actually relatively low in comparison with the high species
richness to be found in sediment systems. So it is relatively
easy for the taxonomic effort to keep pace with the rate of
discovery (although there is a backlog even among seep and
vent fauna). The size of the task facing taxonomists in
nodule fields and off vent areas is a magnitude larger but
the resources to support this work available are actually
less.
The future will depend on maximising the resources we
have, increasing the co-ordination between industry and
academia so that the most is made of the efforts currently
underway and being planned.
12 Dec 2014
6. References
Ahnert, A., Schriever, G., 2001. Response of abyssal
Copepoda Harpacticoida (Crustacea) and other
meiobenthos to an artificial disturbance and its bearing on
future mining for polymetallic nodules. Deep-Sea Research
II, 48, 3779–3794.
Almeida-Neto, M., Guimaraes, P., Guimaraes, P.R., Jr.,
Loyola, R.D., Ulrich, W., 2008. A consistent metric for
nestedness analysis in ecological systems: reconciling
concept and measurement. Oikos, 117 (8), 1227-1239.
Arnds, J., Knittel, K., Boetius, A., Amann, R., 2007. Black Sea
shelf microbial reefs. Geochimica Et Cosmochimica Acta 71
(15), A36-A36.
Bachraty C., Legendre P., Desbruyères D. 2009.
Biogeographic relationships among deep-sea hydrothermal
vent faunas at global scale. Deep Sea Research I, 56,
1371–1378.
Baselga, A. 2010. Partitioning the turnover and nestedness
components of beta diversity. Global Ecology and
Biogeography, 19, 134–143
Bayer, F.M., 1964. The genus Corallium (Gorgonacea :
Scleraxonia) in the western North Atlantic Ocean. Bulletin of
Marine Science of the Gulf and Caribbean, 14 (3), 465-478.
Beerli, P., Felsenstein, J, 1999. Maximum-likelihood
estimation of migration rates and effective population
numbers in two populations using a coalescent approach.
Genetics, 152, 763-773.
Bergstad, O.A., Falkenhaug, T., Astthorsson, O.S., Byrkjedal,
I., Gebruk, A.V., Piatkowski, U., Priede, I.G., Santos, R.S.,
Vecchione, M., Lorance, P., Gordon, J.D.M., 2008. Towards
improved understanding of the diversity and abundance
patterns of the mid-ocean ridge macro- and megafauna.
Deep-Sea Research Part II, 55 (1-2), 1-5.
41
Bergstad, O.A., Gebruk, A.V., 2008. Approach and methods
for sampling of benthic fauna on the 2004 MAR-ECO
expedition to the Mid-Atlantic Ridge. Marine Biology
Research, 4 (1-2), 160-163.
Cairns S.D. (2007) Deep-water corals: an overview with
special reference to diversity and distribution of deepwater
Scleractinian corals. Bulletin of Marine Science, 81,
311–322.
Bongiorni, L,. Ravara, A., Parretti, P., Amaro, T., Cunha, M.R.
2013. Organic matter composition and macrofaunal
diversity in sediments of the Condor Seamount (Azores, NE
Atlantic). Deep-Sea Research II, 98, 75-86.
Carreiro-Silva M., Braga-Henriques, A., Sampaio, I., Matos,
V., Porteiro, F., Ocaña, O. 2011. Isozoanthus primnoidus, a
new zoanthid species (Anthozoa: Hexacorallia) associated
with the gorgonian Callogorgia verticillata (Anthozoa:
Octocorallia) in the Azores. ICES Journal of Marine Science,
68: 408-415.
Braga-Henriques, A., Porteiro, F. M., Ribeiro, P. A., de Matos
V., ´ Sampaio, I., Ocaña O., and Santos, R. S. 2013 Diversity,
distribution and spatial structure of the cold-water coral
fauna of the Azores (NE Atlantic). Biogeosciences, 10,
4009–4036.
Brault, S., Stuart, C.T., Wagstaff, M.C., McClain, C.R., Allen,
J.A., Rex, M.A., 2013a. Contrasting patterns of alpha- and
beta-diversity in deep-sea bivalves of the eastern and
western North Atlantic. Deep-Sea Research Part II, 92,
157-164.
Brault, S., Stuart, C.T., Wagstaff, M.C., Rex, M.A., 2013b.
Geographic evidence for source-sink dynamics in deep-sea
neogastropods of the eastern North Atlantic: an approach
using nested analysis. Global Ecology and Biogeography 22
(4), 433-439.
Brown, C.J. 1998. Effects of phytodetriatal input on
nematode communities of the abyssal equatorial Pacific.
PhD Thesis, University of Southampton, UK. 302pp.
Bunz, S., Polyanov, S., Vadakkepuliyambatta, S., Consolaro,
C., Mienert, J., 2012. Active gas venting through
hydrate-bearing sediments on the Vestnesa Ridge, offshore
W-Svalbard. Marine Geology, 332, 189-197.
Bussau, C., Schriever, G., Thiel R., 1995) Evaluation of
abyssal metazoan meiofauna from a manganese nodule
area of the eastern south Pacific. Vie Milieu, 45(1), 39-48.
Carreiro-Silva M., Ocaña O, Sampaio I, Matos V, Porteiro F
Braga-Henriques A, Steffani (in prep) Zoanthid diversity
associated with cold-water corals in the Azores Region:
evidence for substrate specificity. Marine Biodiversity
CBD, 2009. Azores Scientific criteria and guidance for
identifying ecologically or biologically significant marine
areas and designing representative networks of marine
protected areas in open ocean waters and deep sea
habitats. Convention on Biological Diversity, p. 12.
Collins, P.C., Kennedy, R., Van Dover, C.L., 2012. A biological
survey method applied to seafloor massive sulphides (SMS)
with contagiously distributed hydrothermal-vent fauna.
Marine Ecology Progress Series, 452, 89-107.
Comtet, T., Jollivet, D., Dixon, D.R. 2000. Molecular and
morphological identification of settlement-stage vent
mussel larvae, Bathymodiolus azoricus (Bivalvia: Mytilidae),
preserved in situ at active vent fields on the Mid-Atlantic
Ridge. Limnology and Oceanography, 45 (7). 1655-1661.
Crepeau, V.; Bonavita, M-A. C., Lesongeur, F.; et al.
Diversity and function in microbial mats from the Lucky
Strike hydrothermal vent field. FEMS Microbiology Ecology,
76 (3) 524-540
Cuvelier D., Beesau, J., Ivanenko, V.N., Zeppilli D., Sarradin,
P.M., Sarrazin, J. (2014) First insights into macro-and
meiofaunal colonisation patterns on paired wood/slate
substrata at Atlantic deep-sea hydrothermal vents. Deep
Sea Research Part I, 87:70-81.
Davey, J.W., Hohenlohe, P.A., Etter, P.D., Boone, J.Q.,
Catchen J.M., Blaxter, M.L., 2011. Genome-wide genetic
marker discovery and genotyping using next-generation
sequencing. Nature Reviews Genetics, 12, 499-510.
Desbruyères, D., Olu, K., Colaco, A., Comtet, T., Sarradin,
P.-M., Biscoito, M., Fouquet, Y., 2001. Composition and
distribution of communities associated with oceanic
hydrothermalism at the Azores Triple Junction in the Mid
Atlantic. Boletim do Museu Municipal do Funchal,
Suplemento, 6, 75-110.
Dilman, A.B., 2008. Asteroid fauna of the northern
Mid-Atlantic Ridge with description of a new species
Hymenasterides mironovi sp nov. Marine Biology Research,
4 (1-2), 131-151.
Durisch-Kaiser, E. Klauser, L., Wehrli, B. & Schubert, C. 2005.
Evidence of intense archaeal and bacterial methanotrophic
activity in the black sea water column. Applied and
Environmental Microbiology, 71(12), 8099-8106.
Foucher, J.-P., Westbrook, G.K., Boetius, A., Ceramicola, S.,
Dupre, S., Mascle, J., Mienert, J., Pfannkuche, O., Pierre, C.,
Praeg, D., 2009. Structure and Drivers of Cold Seep
Ecosystems. Oceanography, 22 (1), 92-109.
Gaston, K. J. 1994. Rarity. Chapman & Hall, London. 205pp.
Gebruk, A.V., 2008a. Benthic fauna of the northern
Mid-Atlantic Ridge: results of the MAR-ECO expedition.
Marine Biology Research, 4 (1-2), 1-2.
Gebruk, A.V., 2008b. Holothurians (Holothuroidea,
Echinodermata) of the northern Mid-Atlantic Ridge
collected by the GO Sars MAR-ECO expedition with
descriptions of four new species. Marine Biology Research,
4 (1-2), 48-60.
Gebruk, A.V., Budaeva, N.E., King, N.J., 2010. Bathyal
benthic fauna of the Mid-Atlantic Ridge between the Azores
and the Reykjanes Ridge. Journal of the Marine Biological
Association of the United Kingdom, 90 (1), 1-14.
German, C.R., Parson,L.M., Bougault,F., Coller,D.,
Critchley,M., Dapoigny,A., Day, C., Eardley,D., Fearn,A.,
Flewellen,C., Kirk,R., Klinkhammer,G., Landure,J.Y., Ludford,
E.,Miranda, M.,Needham,H.D., Patching,J., Pearce,R.,
Pelle,H., Radford-knoery, J., Rouse,I., Scott,J., Stoffregen,P.,
Taylor,P., Teare,D., Wynar,J., 1996. Hydrothermal
exploration near the Azores triple junction: tectonic control
of venting at slow-spreading ridges? Earth and Planetary
Science Letters, 138, 93–104.
German, C.R., Ramirez-Llodra, E., Baker, M.C., Tyler, P.A.
and the ChEss Scientific Steering Committee, 2011.
Deep-Water Chemosynthetic Ecosystem Research during
the Census of Marine Life Decade and Beyond: A Proposed
Deep-Ocean Road Map. PLoS ONE, 6(8): e23259.
doi:10.1371/journal.pone.0023259.
Glover, A., Paterson, G., Bett, B., Gage, J., Sibuet, M.,
Sheader, M., Hawkins, L., 2001. Patterns in polychaete
abundance and diversity from the Madeira Abyssal Plain,
northeast Atlantic. Deep-Sea Research Part I, 48 (1),
217-236.
Glover, A., Smith, C., Paterson, G., Wilson, G., Hawkins, L.,
Sheader, M. 2002. Polychaete species diversity in the
central Pacific abyss: local and regional patterns, and
relationships with productivity. Marine Ecology-Progress
Series, 240, 157-169.
Gollner, S., Ivanenko, V.N., Martínez Arbizu P., Bright M.
2010a. Advances in taxonomy, ecology, and biogeography
of Dirivultidae (Copepoda) associated with chemosynthetic
environments in the deep sea. PLoS ONE, 5(8): e9801.
doi:10.1371/journal.pone.0009801
Gollner, S., Riemer, B., Martínez Arbizu, P., Le Bris, N.,
Bright, M. 2010b. Diversity of Meiofauna from the 9°50’N
East Pacific Rise across a gradient of hydrothermal fluid
emissions. PLoS ONE, 5(8): e12321.
doi:10.1371/journal.pone.0012321
Gollner, S., Fontaneto, D., Martínez Arbizu, P. 2011)
Molecular taxonomy confirms morphological classification
of deep-sea hydrothermal vent copepods (Dirivultidae) and
suggests broad physiological tolerance of species and
frequent dispersal along ridges. Marine Biology,
158:221-231. doi: 10.1007/s00227-010-1553-y
Gooday, A. J., Hori, S., Todo Y., Okamoto, T., Kitazato H. &
Sabbatini A. 2004. Soft-walled, monothalamous benthic
foraminiferans in the Pacific, Indian and Atlantic Oceans:
aspects of biodiversity and biogeography. Deep Sea
Research Part I, 51, 33-53,
Grasshoff, M., 1982. Die Gorgonaria, Pennatularia und
Antipatharia des Tiefwassers der Biskaya (Cnidaria,
Anthozoa). Ergebnisse der franzosischen Expeditionen
Biogas, Polygas, Geomanche, Incal, Noratlante und Fahrten
der ‘Thalassa’. 2. Taxonomischer Teil. Bulletin du Museum
National d’Histoire Naturelle Section A Zoologie Biologie et
Ecologie Animales, 3 (4), 941-978.
Grasshoff, M. 1986. Die Gorgonaria de Expeditionen von
“Travailleur” 1880_1882 und “Talisman” 1883 (Cnidaria,
Anthozoa). Bulletin Muséum national d’Histoire Naturelle,
Paris, 4e série, 8, 9-38.
Grigg, R.W., 1994. History of the precious coral fishery in
Hawaii. Precious Corals & Octocoral Research, 3, 1-18.
Henry L.-A., Davies A.J., & Roberts J.M. 2010. Beta diversity
of cold-water coral reef communities off western Scotland.
Coral Reefs, 29,427-436
Hessler, R. R. and P. A. Jumars, 1974. Abyssal community
analysis from replicate box cores in the central North
Pacific, Deep-sea Research 21,185–209.
42
Ivanenko, V.N., Corgosinho, P.H.C., Ferrari, F.D., Sarradin,
P.M., Sarrazin, J. 2012. Microhabitat distribution of
Smacigastes micheli (Copepoda: Harpacticoida: Tegastidae)
from deep-sea hydrothermal vents at the Mid-Atlantic
Ridge, 37°N (Lucky Strike), with a morphological description
of the nauplius. Marine Ecology Evolutionary Perspectiv,e
33(2), 245-256.
Ivanenko, V.N., Defaye, D. 2004. A new and primitive genus
and species of deep-sea Tegastidae (Crustacea, Copepoda,
Harpacticoida) from the Mid-Atlantic Ridge, 37°N (Azores
Triple Junction, Lucky Strike). Cahiers De Biologie Marine,
45, 255-268.
Jain, M., Flynn, D.F.B., Prager, C.M., Hart, G.M., DeVan,
C.M., Ahrestani, F.S., Palmer, M.I., Bunker, D.E., Knops,
J.M.H., Jouseau, C.F., Naeem, S., 2014. The importance of
rare species: a trait-based assessment of rare species
contributions to functional diversity and possible ecosystem
function in tall-grass prairies. Ecology and Evolution, 4 (1),
104-112.
Keller, I., Wagner, C.E., Greuter, L., Mwaiko, S., Selz, O.M.,
Sivasundar, A., Wittwer, S., Seehausen, O. 2013. Population
genomic signatures of divergent adaptation, gene flow and
hybrid speciation in the rapid radiation of Lake Victoria
cichlid fishes. Molecular Ecology, 22, 2848-2863.
Kuypers, M.M. M, Slieker, A.O., Lavik, G, Schmid, M.,
Jorgensem, B.B., Kuenen, J.G., Sinninghe Damste, J.S.,
Strous, M., Jetten, Mike S.M. 2003. Anaerobic ammonium
oxidation by anammox bacteria in the Black Sea. Nature,
422, 608-611.
Lackschewitz, K.S., Endler, R., Gehrke, B., WallrabeAdams,
H.J., Thiede, J., 1996. Evidence for topography- and
current-controlled deposition on the Reykjanes Ridge
between 59 degrees N and 60 degrees N. Deep-Sea
Research Part I, 43 (11-12), 1683-1711.
Lambshead, P.J.D., Brown, C.J., Ferrero, T.J., Hawkins, L.E.,
Smith, C.R., Mitchell, N.J., 2003. Biodiversity of nematode
43
assemblages from the region of the Clarion-Clipperton
Fracture Zone, an area of commercial mining interest. BMC
Ecology 3 (1), Unpaginated.
Le Goff-Vitry, M.C., Pybus, O.G. & Rogers, A.D., 2004.
Genetic structure of the deep-sea coral Lophelia pertusa in
the northeast Atlantic revealed by microsatellites and
internal transcribed spacer sequences. Molecular Ecology,
13, 537-549.
Lecroq, B., Gooday, A.J., Cedhagen, T., Sabbatini, A. ,
Pawlowski, J., 2009a. Molecular analyses reveal high levels
of eukaryotic richness associated with enigmatic deep-sea
protists (Komokiacea). Marine Biodiversity, 39 (1), 45-55.
Lecroq, B., Gooday, A.J. & Pawlowski, J., 2009b. Global
genetic homogeneity in the deep-sea foraminiferan
Epistominella exigua (Rotaliida: Pseudoparrellidae).
Zootaxa, 2096, 23-32.
Lecroq, B., Lejzerowicz, F., Bachar, D., Christen, R., Esling, P.,
Baerlocher, L., Osteras, M., Farinelli, L., Pawlowski, J., 2011.
Ultra-deep sequencing of foraminiferal microbarcodes
unveils hidden richness of early monothalamous lineages in
deep-sea sediments. Proceedings of the National Academy
of Sciences of the United States of America, 108 (32),
13177-13182.
abiogenous origin. Instruments, Methods, and Missions for
Astrobiology, Xiv, 8152.
Magurran, A.E., Henderson, P.A. 2003. Explaining the excess
of rare species in natural species abundance distributions.
Nature, 422: 714-716.
Mahatma, R., 2009. Meiofauna Communities of the Pacific
Nodule Province: Abundance, Diversity and Community
Structure. Ph.D. Thesis. Carl von Ossietzky Universit¨ at,
Oldenburg, 142 pp.
Martynov, A.V., Litvinova, N.M., 2008. Deep-water
Ophiuroidea of the northern Atlantic with descriptions of
three new species and taxonomic remarks on certain
genera and species. Marine Biology Research, 4 (1-2),
76-111.
Maybury, C. 1996. Crevice foraminifera from abyssal south
east Pacific manganese nodules. Microfossils and oceanic
environments, 281-295.
Miljutin, D.M., Miljutina, M.A., Arbizu, P.M., Galeron, J.,
2011. Deep-sea nematode assemblage has not recovered
26 years after experimental mining of polymetallic nodules
(Clarion-Clipperton Fracture Zone, Tropical Eastern Pacific).
Deep-Sea Research Part I, 58 (8), 885-897.
Lejzerowicz, F., Voltsky, I. and Pawlowski, J, 2013.
Identifying active foraminifera in the Sea of Japan using
metatranscriptomic approach. Deep-Sea Research Part II,
86-87, 214-220.
Miljutina, M.A., Miljutin, D.M., 2012. Seven new and four
known species of the genus Acantholaimus (Nematoda:
Chromadoridae) from the abyssal manganese nodule field
(Clarion-Clipperton Fracture Zone, North-Eastern Tropical
Pacific). Helgoland Marine Research, 66 (3), 413-462.
Lichtschlag, A., Felden, J., Wenzhofer, F., Schubotz, F.,
Ertefai, T.F., Boetius, A., de Beer, D., 2010. Methane and
sulfide fluxes in permanent anoxia: In situ studies at the
Dvurechenskii mud volcano (Sorokin Trough, Black Sea).
Geochimica Et Cosmochimica Acta, 74 (17), 5002-5018.
Miljutina, M.A., Miljutin, D.M., Mahatma,R., Galéron, J.
2010. Deep-sea nematode assemblages of th
Clarion-Clipperton Nodule Province (Tropical North-Eastern
Pacific). Marine Biodiversity, 40, 1–15.
Lysyuk, G. N. 2011. Biomineral microstructures in
ferromanganese nodules: evidence of the biological and
Mincks, S. L., Smith, C. R. 2006. Critical Review of Benthic
Biological Data from the Clarion-Clipperton Zone (CCZ) and
Adjoining Areas. Report to the ISA.
Mironov, A.N., 2008. Pourtalesiid sea urchins
(Echinodermata : Echinoidea) of the northern Mid-Atlantic
Ridge. Marine Biology Research, 4 (1-2), 3-24.
Mironov, A.N., Gebruk, A.V. 2006. Biogeography of the
Reykjanes ridge, the northern Atlantic. In Mironova, A.N.,
Gebruk, A.V., Southward, A. J. eds. Biogeography of the
North Atlantic Seamounts. KMK Scientific Press,
Moscow.pp6-21.
Moalic et al, 2012. Biogeography revisited with network
theory: retracing the history of hydrothermal vent
communities. Systematic Biology, 61(1),127–137,
Molodtsova, T.N., Sanamyan, N.P., Keller, N.B., 2008.
Anthozoa from the northern Mid-Atlantic Ridge and
Charlie-Gibbs fracture zone. Marine Biology Research, 4
(1-2), 112-130.
Morato, T., Pitcher, T.J., Clark, M.R., Menezes, G., Tempera,
F., Porteiro, F., Giacomello, E., Santos, R.S., 2010. Can We
Protect Seamounts for Research? A call for conservation.
Oceanography, 23 (1), 190-199.
Mouillot, D., Bellwood, D.R., Baraloto, C., Chave, J., Galzin,
R., Harmelin-Vivien, M., Kulbicki, M., Lavergne, S., Lavorel,
S., Mouquet, N., Paine, C.E.T., Renaud, J., Thuiller, W.,
2013a. Rare Species Support Vulnerable Functions in
High-Diversity Ecosystems. PLoS Biology 11 (5), 1-11.
Mullineaux L.S. (1987) Organisms living on manganese
nodules and crusts: distribution and abundance at three
North Pacific sites. Deep Sea Research, 34, 165-184.
Murton,B.J.,Klinkhammer,G.,Becker,K.,Briais,A.,Edge,D.,Hay
ward,N.,Millard,N., Mitchell,I., Rouse,I., Rudnick,M.,
Sayanagi,K., Sloan,H., Parson,L.,1994. Direct evidence for
the distribution and occurrence of hydrothermal activity
between 27°-30°N on the Mid-Atlantic Ridge. Earth
Planetary Science Letters,125,119–128.
Naheem, S. 1998. Species redundancy and ecosystem
reliability. Conservation Biology, 12, 39-45.
Nimmo M, Morgan C and Banning D, 2013.
Clarion-Clipperton Zone Project, Pacific Ocean: UPDATED NI
43-101 Technical Report. 127631013-003-R-Rev1.
Nozawa, F., Kitazato, H., Tsuchiya, M., Gooday, A. J. 2006.
‘Live’ benthic foraminifera at an abyssal site in the
equatorial Pacific nodule province: Abundance, diversity
and taxonomic composition. Deep-Sea Research Part I, 53,
1406-1422.
Priede, I.G., Bergstad, O.A., Miller, P.I., Vecchione, M.,
Gebruk, A., et al. 2013. Does Presence of a Mid-Ocean Ridge
Enhance Biomass and Biodiversity? PLoS ONE, 8(5): e61550.
doi:10.1371/journal.pone.0061550
Quattrini A.M., Etnoyer P.J., Doughty C., English L., Falco R.,
Remon N., Rittinghouse M., Cordes E.E. 2014. A
phylogenetic approach to octocoral community structure in
the deep Gulf of Mexico. Deep Sea Research Part II, 99,
92-102.
R Development Core Team, 2006.
O’mullan et al, 2001. A hybrid zone between hydrothermal
vent mussels (Bivalvia: Mytilidae) from the Mid-Atlantic
Ridge. Molecular Ecology, 10, 2819-2831
Radziejewska, T., 2002. Responses of deep-sea meiobenthic
communities to sediment disturbance simulating effects of
polymetallic nodule mining. International Review of
Hydrobiology, 87 (4), 457-477.
Pante, E,, Abdelkrim, J., Viricel, A., Gey, D., France, S.C.,
Boisselier, M-C., Samadi, S, online proof. Use of RAD
sequencing for delimiting species.
https://hal.archives-ouvertes.fr/hal-01064545/.
Radziejewska, T. 2014. Meiobenthos in the sub-equatorial
Pacific abyss. Springer, Hedelberg. 105pp.
Paterson, G., Wilson, G., Cosson, N., Lamont, P. 1998.
Hessler and Jumars (1974) revisited: abyssal polychaete
assemblages from the Atlantic and Pacific. Deep-Sea
Research Part II, 45 (1-3), 225-251.
Pawlowski, J., Fontaine, D., da Silva, A.A., Guiard, J. 2011.
Novel lineages of Southern Ocean deep-sea foraminifera
revealed by environmental DNA sequencing. Deep-Sea
Research Part II, 58 (19-20), 1996-2003.
Pawlowski, J., Holzmann, M. 2008. Diversity and geographic
distribution of benthic foraminifera: a molecular
perspective. Biodiversity and Conservation, 17 (2), 317-328.
Petersen, J.M., Ramette, A., Lott, C., Cambon-Bonavita,
M.A., Zbinden, M., Dubilier, N. 2010. Dual symbiosis of the
vent shrimp Rimicaris exoculata with filamentous Gammaand Epsilonproteobacteria at four Mid-Atlantic Ridge
hydrothermal vent fields. Environmental Microbiology, 12,
2204–2218.
Radziejewska, T., I. Drzycimski, V. V. Galtsova, L. V.
Kulangieva and V. Stoyanova, 2001a. Changes in genus-level
diversity of meiobenthic free living nematodes (Nematoda)
and harpacticoids (Copepoda: Harpacticoida) at an abyssal
site following experimental sediment disturbance,
Proceeding of the Fourth Ocean Mining Symposium,
Szczccin, Poland, September 23–27, pp. 38–43
Radziejewska, T. and I. Modlitba, 1999, Vertical distribution
of meiobenthos in relation to geotechnical properties of
deep-sea sediment in IOM pioneer area (Clarion-Clipperton
Fracture Zone, NE Pacific), Proceeding of the Third Ocean
Mining Symposium, pp. 126–130.
Radziejewska, T., Stoyanova, V., 2000. Abyssal epibenthic
megafauna of the Clarion-Clipperton area (NE Pacific):
changes in time and space versus anthropogenic
environmental disturbance. Oceanological Studies, 29 (2),
83-101.
44
Renaud-Mornant, J., Gourbault, N., 1990. Evaluation of
abyssal meiobenthos in the eastern central Pacific
(Clarion-Clipperton Fracture-Zone). Progress in
Oceanograph,y 24 (1-4), 317-329.
Riedel A., Sagata K., Suhardjono Y.R., Tänzler, R., Balke, M.
2013. Integrative taxonomy on the fast track – towards
more sustainability in biodiversity research. Frontiers in
Zoology, 10,15.
Riemann, F. 1983. Biological Aspects Of Deep-Sea
Manganese-Nodule Formation. Oceanologica Acta, 6,
303-311.
Sampaio, I., Oca˜na, O., Tempera, F., Braga-Henriques, A.,
Matos, V., & Porteiro, F. New occurrences of Corallium spp.
(Octocorallia, Coralliidae) in the Central Northeast Atlantic,
Archipelago, Life Marine Science, 26, 73–78, 2009.
dos Santos, E., Nolso, A., Schander, C., Tendal, O.S.,
Ragnarsson, S.A., Svavarrsson, J., 2009. Deep-water
communities in the West-Nordic area. TemaNord, 529,
1-44.
Schöttner, S. et al. Inter- and intra-habitat bacterial diversity
associated with cold-water corals. ISME J. 3, 756–759
(2009).
Schröder, C. J., Scott, D. B., Medioli, F. S., Bernstein, B. B. ,
Hessler, R. R. 1988. Larger agglutinated foraminifera comparison of assemblages from central north pacific and
western north-atlantic (nares abyssal-plain). Journal of
Foraminiferal Research, 18, 25-41.
Shank, T. M., Halanych, K. M. 2007. Toward a mechanistic
under-standing of larval dispersal: insights from genomic
fingerprinting of deep-sea hydrothermal vent populations.
Marine Ecology, 28, 25 – 35.
Shields, M.A., Blanco-Perez, R., 2013. Polychaete
abundance, biomass and diversity patterns at the
45
Mid-Atlantic Ridge, North Atlantic Ocean. Deep-Sea
Research Part II, 98, 315-325.
Smith, C. R., Berelson, W., Demaster, D. J., Dobbs, F. C.,
Hammond, D., Hoover, D. J., Pope, R. H. & Stephens, M.
1997. Latitudinal variations in benthic processes in the
abyssal equatorial Pacific: control by biogenic particle flux.
Deep-Sea Research Part II, 44, 2295-.
Smith, C. R., Hoover, D. J., Doan, S. E., Pope, R. H.,
Demaster, D. J., Dobbs, F. C. & Altabet, M. A. 1996.
Phytodetritus at the abyssal seafloor across 10 degrees of
latitude in the central equatorial Pacific. Deep-Sea Research
Part II, 43, 1309-1338.
Smith CR, et al. (2008) Biodiversity, species ranges, and
gene flow in the abyssal Pacific nodule province: predicting
and managing the impacts of deep seabed mining.Technical
Study No. 3. Kingston, Jamaica: International Seabed
Authority.38pp
Snider, L.J., Burnett, B.R., Hessler, R.R., 1984. The
composition and distribution of meiofauna and nanobiota in
a central north Pacific deep-sea area. Deep-Sea Research
Part A, 31 (10), 1225-1249.
Tabachnick, K.R. & Collins, A.G., 2008. Glass sponges
(Porifera, hexactinellida) of the northern mid-Atlantic Ridge.
Marine Biology Research, 4 (1-2), 25-47.
Teixeira S., Cambon-Bonavita, M.-A. et al. 2011. Recent
population expansion and connectivity in the hydrothermal
shrimp Rimicaris exoculata along the Mid Atlantic Ridge.
Journal of Biogeography, 38, 564-574.
Teixeira S., Serra˜o E.A. & Arnaud-Haond, S. 2012. Panmixia
in a fragmented and unstable environment: the
hydrothermal shrimp Rimicaris exoculata disperses
extensively along the Mid-Atlantic Ridge. PLoS ONE, 7(6):
e38521. doi:10.1371/journal.pone.0038521
Thiel H., Schriever G., Bussau C., Borowski C. 1993.
Manganese nodule crevice fauna. Deep Sea Research I, 40:
419-423.
Tilot, V. 2006. Biodiversity and distribution of the
megafauna. Vol 1. The polymetallic nodule ecosystem of
the echinoderms of the Clarion-Clipperton fracture zone.
eastern Equatorial Pacific Ocean. Vol 2. Annotated
photographic atlas1995. An ecologically important type of
biological activity in a deep-sea ferro-manganese nodule
environment of the tropical north east Pacific. UNESCO/IOC
(IOC Technical series 69).
Tittensor, D.P., Baco, A.R., Brewin, P.E., Clark, M.R.,
Consalvey, M., Hall-Spencer, J., Rowden, A.A., Schlacher, T.,
Stocks, K.I., Rogers, A.D., 2009. Predicting global habitat
suitability for stony corals on seamounts. Journal of
Biogeography, 36 (6), 1111-1128.
Tully, B. J. & Heidelberg, J. F. 2013. Microbial communities
associated with ferromanganese nodules and the
surrounding sediments. Frontiers in Microbiology, 4.
Vafidis, D,, Koukouras, A., Voultsiadou-Koukoura, E. 1994.
Octocoral fauna of the Aegean Sea with a check list of the
Mediterranean species: new information, faunal
comparisons. Annales de l’Institut oceanographique,
Nouvelle serie, 70 (2), 217-229.
van der Heijden K., Petersen, J.M., Dubilier, N., Borowski, C.
2012. Genetic Connectivity between North and South
Mid-Atlantic Ridge Chemosynthetic bivalves and their
symbionts. PLoS ONE, 7(7): e39994.
Van Dover, C.L. 1988. Recruitment of marine invertebrates
to hard substates at deep-sea hydrothermal vents onthe
East Pacific Rise ad Galapagos spreading centre. Deep Sea
Research, Part A. 35, 1833-1849.
Van Dover, C.L. 2012. Hydrothermal vent ecosystems and
consevation. Oceanography, 25, 313-316.
VanDover, C.L., Desbruyeres, D., Segonzac, M., Comtet, T.,
Saldanha, L., FialaMedioni, A., Langmuir, C., 1996. Biology of
the Lucky Strike hydrothermal field. Deep-Sea Research Part
I, 43 (9), 1509-&.
Van Dover, C.L., Doerries, M.B. 2005. Community structure
in mussel beds at Logatchev hydrothermal vents and a
comparison of macrofauna species richness on slow and
fast-spreading mid-ocean ridges. Marine Ecology, 26,
110-120.
Van Dover, C.L., German, C., Speer, K.G., Parson, L.M. &
Vrijenhoek R.C. 2002. Evolution and biogeography of
deepsea vent and seep invertebrates. Science, 295,
1253–1257.
Vanreusel, A., Andersen, A.C., Boetius, A., Connelly, D.,
Cunha, M.R., Decker, C., Hilario, A., Kormas, K.A., Maignien,
L., Olu, K., Pachiadaki, M., Ritt, B., Rodrigues, C., Sarrazin, J.,
Tyler, P., Van Gaever, S., Vanneste, H., 2009. Biodiversity of
cold seep ecosystems along the European Margins.
Oceanography, 22 (1), 110-127.
Veillette, J., Juniper, S. K., Gooday, A. J., Sarrazin, J. 2007a.
Influence of surface texture and microhabitat heterogeneity
in structuring nodule faunal communities. Deep-Sea
Research Part I, 54, 1936-1943.
Veillette, J., Sarrazin, J., Gooday, A. J., Galeron, J., Caprais, J.
C., Vangriesheim, A., Etoubleau, J., Christian, J. R., Juniper,
S. K. 2007b. Ferromanganese nodule fauna in the Tropical
North Pacific Ocean: Species richness, faunal cover and
spatial distribution. Deep-Sea Research Part I, 54,
1912-1935.
Verlaan, P. A. 1992. Benthic recruitment and manganese
crust formation on seamounts. Marine Biology, 113,
171-174.
Vierod, A.D.T., Guinotte, J.M., Davies, A.J., 2014. Predicting
the distribution of vulnerable marine ecosystems in the
deep sea using presence-background models. Deep Sea
Research Part II, 99, 6-18.
Vogler, A.P., Monaghan, M.T., 2007. Recent advances in
DNA taxonomy. Journal of Zoological Systematics and
Evolutionary Research, 45, 1-10.
Vopel, K., Thiel, H., 2001. Abyssal nematode assemblages in
physically disturbed and adjacent sites of the eastern
equatorial Pacific. Deep-Sea Research Part II, 48,
3795–3808.
Wang, c. S., Liao, L., Xu, H. X., Xu, X. W., Xu, M., Zhu, l. Z.
2010. Bacterial Diversity in the Sediment from Polymetallic
Nodule Fields of the Clarion-Clipperton Fracture Zone.
Journal of Microbiology, 48, 573-585.
Wang, X., Schroeder, H. C., Schlossmacher, U., Mueller, W.
E. G. 2009b. Organized bacterial assemblies in manganese
nodules: evidence for a role of S-layers in metal deposition.
Geo-Marine Letters, 29, 85-91.
Watling, L., Auster, P.J. (2005) Distribution of deep-water
Alcyonacea off the northeast coast of the United States. In
Cold-Water Corals and Ecosystems (A. Freiwald and J. M.
Roberts, eds), pp. 279_296. Springer-Verlag, Berlin.
Wedding, L.M., Friedlander, A.M., Kittinger, J.N., Watling, L.,
Gaines, S.D., Bennett, M., Hardy, S.M., Smith, C.R.,2013.
From principles to practice: a spatial approach to systematic
conservation planning in the deep sea. Proceedings of the
Royal Society B, Biological Sciences, 280 1471-2954.
doi:10.1098/rspb.2013.1684
Willette, D.A., Allendorf FW, Barber PH, Barshis DJ,
Carpenter KE, Crandall ED, Cresko WA, Fernandez-Silva I,
Matz MV, Meyer E, Santos MD, Seeb LW and Seeb JE, 2014.
So, you want to use next-generation sequencing in marine
systems? Insight from the Pan-Pacific Advanced Studies
Institute. Bulletin of Marine Science, 90, 79-122.
Won, Y.-J., Hallam, S. J., O’Mullan, G.D., Pan, I. L., Buck, K.
R., Vrijenhoek, R. C. 2003. Environmental Acquisition of
Thiotrophic Endosymbionts by Deep-Sea Mussels of the
Genus Bathymodiolus Applied Environmental Microbiology,
2003, 69(11),6785.
Wu, Y.-H., Liao, L., Wang, C.-S., Ma, W.-L., Meng, F.-X., Wu,
M., Xu, X.-W. 2013. A comparison of microbial communities
in deep-sea polymetallic nodules and the surrounding
sediments in the Pacific Ocean. Deep-Sea Research Part I,
79, 40-49.
Xu, M. X., Wang, P., Wang, F. P., Xiao, X. 2005. Microbial
diversity at a deep-sea station of the Pacific nodule
province. Biodiversity and Conservation, 14, 3363-3380.
Xu, M., Wang, F., Meng, J., Xiao, X. 2007. Construction and
preliminary analysis of a metagenomic library from a
deep-sea sediment of east Pacific Nodule Province. Fems
Microbiology Ecology, 62, 233-241.
Zekely, J., Van Dover, C.L., Nemeschkal, H.L., Bright, M.
2006a. Hydrothermal vent meiobenthos associated with
mytilid mussel aggregations from the mid-atlantic ridge and
the east pacific rise. Deep-Sea Research Part I, 53,
1363-1378.
Zekely, J., Sørensen, M.V. & Bright, M. 2006b. Three new
nematode species (Monhysteridae) from deep-sea
hydrothermal vents. Meiofauna Marina, 15, 25-42.
Zeppilli, D., Bongiorni, L., Cattaneo, A., Danovaro, R.,
Santos, R. 2013. Meiofauna assemblages of the Condor
Seamount (North-East Atlantic Ocean) and adjacent
deep-sea sediments. Deep-sea Research Part II, 98, 87-100.
46
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